Stem cells and lineages of the intestine: a developmental and evolutionary perspective

Takashima, Shigeo; Gold, David; Hartenstein, Volker

doi:10.1007/s00427-012-0422-8

Cited by 67Developmental Biology and Gene RegulationDigestive system and related healthMarine Invertebrate Physiology and Ecology

Stem cells and lineages of the intestine: a developmental and evolutionary perspective

Open access

Takashima, Shigeo, Gold, David, Hartenstein, Volker·2013·Development Genes and Evolution

DOI 10.1007/s00427-012-0422-8PMC PMC3873164

Open this paper in CoChat — free account

Abstract

The intestine consists of epithelial cells that secrete digestive enzymes and mucus (gland cells), absorb food particles (enterocytes), and produce hormones (endocrine cells). Intestinal cells are rapidly turned over and need to be replaced. In cnidarians, mitosis of differentiated intestinal cells accounts for much of the replacement; in addition, migratory, multipotent stem cells (interstitial cells) contribute to the production of intestinal cells. In other phyla, intestinal cell replacement is solely the function of stem cells entering the gut from the outside (such as in case of the neoblasts of platyhelminths) or intestinal stem cells located within the midgut epithelium (as in both vertebrates or arthropods). We will attempt in the following to review important aspects of midgut stem cells in different animal groups: where are they located, what types of lineages do they produce, and how do they develop. We will start out with a comparative survey of midgut cell types found across the animal kingdom; then briefly look at the specification of these cells during embryonic development; and finally focus on the stem cells that regenerate midgut cells during adult life. In a number of model systems, including mouse, zebrafish and Drosophila, the molecular pathways controlling intestinal stem cells proliferation and the specification of intestinal cell types are under intensive investigation. We will highlight findings of the recent literature, focusing on aspects that are shared between the different models and that point at evolutionary ancient mechanisms of intestinal cell formation.

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

Crossref · 10.1007/s00427-012-0422-8

Cites

136 of 136 references verified0 citation errors · 0 not checkable

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?

The invention of the mucociliary sole was likely paralleled by cell-type diversification specializing in mucus production, digestive enzyme secretion, mucus transport, and dissolved nutrient uptake.
“The invention of the mucociliary sole was likely paralleled by cell-type diversification (figure 4d), specializing in the production of mucus, the secretion of digestive enzymes, the transport of mucus and the uptake of dissolved nutrients [45].”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [45]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Physiology of the Gastrointestinal Tract
Johnson, L. R. (2006) · Elsevier eBooks · doi:10.1016/b978-0-12-088394-3.x5000-4 · Cited by 4,611 · see citing works
Transmission Electron Microscopy
Williams, D. B., & Carter, C. B. (2009) · Springer eBooks · doi:10.1007/978-0-387-76501-3 · Cited by 4,004 · see citing works
Microscopic anatomy of invertebrates
Harrison, F. W. (1991) · Wiley-Liss eBooks · Cited by 2,736 · see citing works
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 · see citing works
Physiology of the Gastrointestinal Tract.
(1982) · Annals of Internal Medicine · doi:10.7326/0003-4819-96-1-132_3 · Cited by 1,988 · see citing works
Tie2/Angiopoietin-1 Signaling Regulates Hematopoietic Stem Cell Quiescence in the Bone Marrow Niche
Arai, F., Hirao, A., Ohmura, M., Sato, H., Matsuoka, S., Takubo, K., Ito, K., Koh, G. Y., & Suda, T. (2004) · Cell · doi:10.1016/j.cell.2004.07.004 · Cited by 1,958 · see citing works
Notch/γ-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells
van Es, J. H., van Gijn, M. E., Riccio, O., van den Born, M., Vooijs, M., Begthel, H., Cozijnsen, M., Robine, S., Winton, D. J., Radtke, F., et al. (2005) · Nature · doi:10.1038/nature03659 · Cited by 1,541 · see citing works
Coexistence of Quiescent and Active Adult Stem Cells in Mammals
Li, L., & Clevers, H. (2010) · Science · doi:10.1126/science.1180794 · Cited by 1,247 · see citing works
Control of endodermal endocrine development by Hes-1
Jensen, J. N., Pedersen, E. E., Galante, P. E., Hald, J., Heller, R. S., Ishibashi, M., Kageyama, R., Guillemot, F., Serup, P., & Madsen, O. D. (2000) · Nature Genetics · doi:10.1038/71657 · Cited by 1,155 · see citing works
Evidence that stem cells reside in the adult Drosophila midgut epithelium
Micchelli, C. A., & Perrimon, N. (2005) · Nature · doi:10.1038/nature04371 · Cited by 1,139 · see citing works
The adult Drosophila posterior midgut is maintained by pluripotent stem cells
Ohlstein, B., & Spradling, A. C. (2005) · Nature · doi:10.1038/nature04333 · Cited by 1,089 · see citing works
Cytokine/Jak/Stat Signaling Mediates Regeneration and Homeostasis in the Drosophila Midgut
Jiang, H., Patel, P. H., Kohlmaier, A., Grenley, M. O., McEwen, D. G., & Edgar, B. A. (2009) · Cell · doi:10.1016/j.cell.2009.05.014 · Cited by 1,017 · see citing works
Notch signals control the fate of immature progenitor cells in the intestine
Fré, S., Huyghe, M., Mourikis, P., Robine, S., Louvard, D., & Artavanis‐Tsakonas, S. (2005) · Nature · doi:10.1038/nature03589 · Cited by 936 · see citing works
Requirement of Math1 for Secretory Cell Lineage Commitment in the Mouse Intestine
Yang, Q., Bermingham, N. A., Finegold, M. J., & Zoghbi, H. Y. (2001) · Science · doi:10.1126/science.1065718 · Cited by 919 · see citing works
The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo.
Weigel, D., Jürgens, G., Küttner, F., Seifert, E., & Jäckle, H. (1989) · Cell · doi:10.1016/0092-8674(89)90133-5 · Cited by 794 · see citing works
Microscopic Anatomy of Invertebrates
GHIRADELLA, H. T. (1998) · Medical Entomology and Zoology · Cited by 775 · see citing works
Organizing cell renewal in the intestine: stem cells, signals and combinatorial control
Crosnier, C., Stamataki, D., & Lewis, J. H. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1840 · Cited by 756 · see citing works
Multipotent Drosophila Intestinal Stem Cells Specify Daughter Cell Fates by Differential Notch Signaling
Ohlstein, B., & Spradling, A. C. (2007) · Science · doi:10.1126/science.1136606 · Cited by 651 · see citing works
Wnt/β-Catenin Is Essential for Intestinal Homeostasis and Maintenance of Intestinal Stem Cells
Fevr, T., Robine, S., Louvard, D., & Huelsken, J. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01034-07 · Cited by 650 · see citing works
The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins
Ang, S.-L., Wierda, A., Wong, D., Stevens, K. A., Cascio, S., Rossant, J., & Zaret, K. S. (1993) · Development · doi:10.1242/dev.119.4.1301 · Cited by 618 · cited 1× · see citing works
“Several members of this family, such as HNF3b, is already expressed in the endoderm of gastrulating mouse embryos (Ang et al. 1993).”
Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium
Jenny, M., Uhl, C., Roche, C., Duluc, I., Guillermin, V., Guillemot, F., Jensen, J. N., Kédinger, M., & Gradwohl, G. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf649 · Cited by 488 · see citing works
The Role of Maternal VegT in Establishing the Primary Germ Layers in Xenopus Embryos
Zhang, J., Houston, D. W., King, M. L., Payne, C., Wylie, C. C., & Heasman, J. (1998) · Cell · doi:10.1016/s0092-8674(00)81592-5 · Cited by 470 · see citing works
The Development of Cellular Junctions in the Drosophila Embryo
Tepaß, U., & Hartenstein, V. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1054 · Cited by 461 · see citing works
Self-citation
EGFR/Ras/MAPK Signaling Mediates Adult Midgut Epithelial Homeostasis and Regeneration in Drosophila
Jiang, H., Grenley, M. O., Bravo, M. J., Blumhagen, R. Z., & Edgar, B. A. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.11.026 · Cited by 455 · see citing works
The Tumor Suppressors Brat and Numb Regulate Transit-Amplifying Neuroblast Lineages in Drosophila
Bowman, S. K., Rolland, V., Betschinger, J., Kinsey, K. A., Emery, G., & Knoblich, J. A. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.03.004 · Cited by 444 · see citing works
Current View: Intestinal Stem Cells and Signaling
Scoville, D. H., Sato, T., He, X., & Li, L. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.01.079 · Cited by 416 · see citing works
Investigating the origins of triploblasty: `mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa)
Martindale, M. Q., Pang, K., & Finnerty, J. R. (2004) · Development · doi:10.1242/dev.01119 · Cited by 396 · see citing works
Mesenchymal Cells of the Intestinal Lamina Propria
Powell, D. W., Pinchuk, I. V., Saada, J. I., Chen, X., & Mifflin, R. C. (2011) · Annual Review of Physiology · doi:10.1146/annurev.physiol.70.113006.100646 · Cited by 388 · see citing works
Patterning of the Drosophila nervous system: the achaete-scute gene complex
Campuzano, S., & Modolell, J. (1992) · Trends in Genetics · doi:10.1016/0168-9525(92)90234-u · Cited by 382 · see citing works
Wnt Signaling, Lgr5, and Stem Cells in the Intestine and Skin
Haegebarth, A., & Clevers, H. C. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.080758 · Cited by 360 · see citing works
Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells
Lin, G., Xu, N., & Xi, R. (2008) · Nature · doi:10.1038/nature07329 · Cited by 344 · see citing works
Transcription Factor Hepatocyte Nuclear Factor 6 Regulates Pancreatic Endocrine Cell Differentiation and Controls Expression of the Proendocrine Gene ngn3
Jacquemin, P., Durviaux, S. M., Jensen, J. N., Godfraind, C., Gradwohl, G., Guillemot, F., Madsen, O. D., Carmeliet, P., Dewerchin, M. A., Collen, D., et al. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.12.4445-4454.2000 · Cited by 326 · see citing works
Regulatory peptides in fruit fly midgut
Veenstra, J. A., Agricola, H., & Sellami, A. (2008) · Cell and Tissue Research · doi:10.1007/s00441-008-0708-3 · Cited by 325 · see citing works
Minireview: Development and Differentiation of Gut Endocrine Cells
Schonhoff, S. E., Giel-Moloney, M., & Leiter, A. B. (2004) · Endocrinology · doi:10.1210/en.2004-0051 · Cited by 322 · see citing works
Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways
Ren, F., Wang, B., Yue, T., Yun, E.-Y., Ip, Y. T., & Jiang, J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012759107 · Cited by 316 · see citing works
The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration
Karpowicz, P. A., Perez, J. N., & Perrimon, N. (2010) · Development · doi:10.1242/dev.060483 · Cited by 314 · see citing works
Mutant Neurogenin-3 in Congenital Malabsorptive Diarrhea
Wang, J., Cortina, G. R., Wu, S. V., Tran, R. K., Cho, J., Tsai, M., Bailey, T. J., Jamrich, M., Ament, M. E., Treem, W. R., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa054288 · Cited by 313 · see citing works
GATA transcription factors as potentiators of gut endoderm differentiation
Bossard, P., & Zaret, K. S. (1998) · Development · doi:10.1242/dev.125.24.4909 · Cited by 313 · see citing works
The Hippo pathway regulates intestinal stem cell proliferation duringDrosophilaadult midgut regeneration
Shaw, R. L., Kohlmaier, A., Polesello, C., Veelken, C., Edgar, B. A., & Tapon, N. (2010) · Development · doi:10.1242/dev.052506 · Cited by 304 · see citing works
The gastrointestinal tract stem cell niche
Yen, T., & Wright, N. A. (2006) · Stem Cell Reviews and Reports · doi:10.1007/s12015-006-0048-1 · Cited by 279 · see citing works
Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identityPreprint
Lee, C. S., Perreault, N., Brestelli, J. E., & Kaestner, K. H. (2002) · Genes & Development · doi:10.1101/gad.985002 · Cited by 277 · see citing works
Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine
Crosnier, C., Vargesson, N., Gschmeissner, S., Ariza‐McNaughton, L., Morrison, A., & Lewis, J. H. (2005) · Development · doi:10.1242/dev.01644 · Cited by 262 · see citing works
Cell cycle kinetics and development of Hydra attenuata: I. epithelial cells
David, C. N., & Campbell, R. D. (1972) · Journal of Cell Science · doi:10.1242/jcs.11.2.557 · Cited by 257 · see citing works
Spindle Orientation Bias in Gut Epithelial Stem Cell Compartments Is Lost in Precancerous Tissue
Quyn, A. J., Appleton, P. L., Carey, F. A., Steele, R. J. C., Barker, N., Clevers, H., Ridgway, R. A., Sansom, O. J., & Näthke, I. S. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2009.12.007 · Cited by 242 · see citing works
Cell cycle kinetics and development of Hydra attenuata: III. nerve and nematocyte differentiation
David, C. N., & Gierer, A. (1974) · Journal of Cell Science · doi:10.1242/jcs.16.2.359 · Cited by 233 · see citing works
EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells
Xu, N., Wang, S. Q., Tan, D., Gao, Y., Lin, G., & Xi, R. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.03.018 · Cited by 217 · see citing works
Developmental Competence of the Gut Endoderm: Genetic Potentiation by GATA and HNF3/Fork Head Proteins
Zaret, K. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9228 · Cited by 209 · see citing works
end-1 encodes an apparent GATA factor that specifies the endoderm precursor in Caenorhabditis elegans embryosPreprint
Zhu, J., Hill, R. J., Heid, P. J., Fukuyama, M., Sugimoto, A., Priess, J. R., & Rothman, J. H. (1997) · Genes & Development · doi:10.1101/gad.11.21.2883 · Cited by 208 · see citing works
The morphology and fine structure of the larval midgut of a moth (Manduca sexta) in relation to active ion transport
Cioffi, M. (1979) · Tissue and Cell · doi:10.1016/0040-8166(79)90057-0 · Cited by 191 · see citing works
CELL CYCLE KINETICS AND DEVELOPMENT OF HYDRA ATTENUATA
David, C. N., & Campbell, R. D. (1974) · Open access LMU (Ludwid Maxmilian's Universitat Munchen) · Cited by 189 · see citing works
Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms
Nakanishi, N., Renfer, E., Technau, U., & Rentzsch, F. (2012) · Development · doi:10.1242/dev.071902 · Cited by 188 · see citing works
Transcriptional control of stem cell maintenance in the Drosophila intestine
Bardin, A. J., Perdigoto, C. N., Southall, T. D., et al. (2010) · Development · doi:10.1242/dev.039404 · Cited by 186 · see citing works
Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation
Lee, W.-C., Beebe, K., Sudmeier, L. J., & Micchelli, C. A. (2009) · Development · doi:10.1242/dev.035196 · Cited by 181 · see citing works
Drosophila midgut homeostasis involves neutral competition between symmetrically dividing intestinal stem cells
de Navascués, J., Perdigoto, C. N., Bian, Y., Schneider, M., Bardin, A. J., Martínez-Arias, A., & Simons, B. D. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.106 · Cited by 180 · see citing works
Regulation of self-renewal and differentiation by the intestinal stem cell niche
Yeung, T. M., Chia, L. A., Kosinski, C., & Kuo, C. J. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0687-5 · Cited by 177 · see citing works
The planarian neoblast: the rambling history of its origin and some current black boxes
Baguñ, J. (2012) · The International Journal of Developmental Biology · doi:10.1387/ijdb.113463jb · Cited by 173 · see citing works
SRC-1 and Wnt Signaling Act Together to Specify Endoderm and to Control Cleavage Orientation in Early C. elegans Embryos
Bei, Y., Hogan, J. D., Berkowitz, L. A., Soto, M. C., Rocheleau, C. E., Pang, K. M., Collins, J., & Mello, C. C. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00185-5 · Cited by 164 · see citing works
Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalianachaete-scuteandatonalhomologs in cultured neural progenitor cells
Lo, L., Dormand, E., Greenwood, A. L., & Anderson, D. J. (2002) · Development · doi:10.1242/dev.129.7.1553 · Cited by 158 · see citing works
Notch Lineages and Activity in Intestinal Stem Cells Determined by a New Set of Knock-In Mice
Fré, S., Hannezo, É., Šale, S., Huyghe, M., Lafkas, D., Kissel, H., Louvi, A., Greve, J. M., Louvard, D., & Artavanis‐Tsakonas, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025785 · Cited by 155 · see citing works
Patterning of the Drosophila nervous system: the achaete-scute gene complex
Campuzano, S. (1992) · Trends in Genetics · doi:10.1016/0168-9525(92)90099-p · Cited by 155 · see citing works
Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians
Shibata, N., Rouhana, L., & Agata, K. (2010) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01155.x · Cited by 149 · see citing works
The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea.
Seipel, K., Yanze, N., & Schmid, V. J. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.15005568 · Cited by 143 · see citing works
Repression of mesodermal fate byfoxa, a key endoderm regulator of the sea urchin embryo
Oliveri, P., Walton, K. D., Davidson, E. H., & McClay, D. R. (2006) · Development · doi:10.1242/dev.02577 · Cited by 141 · see citing works
Vertebrate bHLH Genes and the Determination of Neuronal Fates
Guillemot, F. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4717 · Cited by 141 · see citing works
Genetic mechanisms of early neurogenesis inDrosophila melanogaster
Campos-Ortega, J. A. (1995) · Molecular Neurobiology · doi:10.1007/bf02740668 · Cited by 137 · see citing works
Asymmetric developmental potential along the animal–vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled
Lee, P. N., Kumburegama, S., Marlow, H. Q., Martindale, M. Q., & Wikramanayake, A. H. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.05.040 · Cited by 135 · see citing works
The Role of the Visceral Mesoderm in the Development of the Gastrointestinal Tract
McLin, V. A., Henning, S., & Jamrich, M. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.03.001 · Cited by 129 · see citing works
Interpreting epithelial cancer biology in the context of stem cells: Tumor properties and therapeutic implications
Miller, S. J., Lavker, R. M., & Sun, T. (2005) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2005.07.003 · Cited by 128 · see citing works
A two-step model for the fate determination of presumptive endodermal blastomeres in Xenopus embryos
Yasuo, H., & Lemaire, P. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80391-1 · Cited by 126 · see citing works
Stem cell-based growth, regeneration, and remodeling of the planarian intestine
Forsthoefel, D. J., Park, A. E., & Newmark, P. A. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.05.669 · Cited by 125 · see citing works
A role for GATA5 in Xenopus endoderm specification
Weber, H., Symes, C. E., Walmsley, M. E., Rodaway, A., & Patient, R. K. (2000) · Development · doi:10.1242/dev.127.20.4345 · Cited by 121 · see citing works
Copper cells and stomach acid secretion in the Drosophila midgut
Dubreuil, R. R. (2003) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2003.07.004 · Cited by 116 · see citing works
Totipotent migratory stem cells in a hydroid
Müller, W. A., Teo, R., & Frank, U. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.08.006 · Cited by 116 · see citing works
Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia
Leclère, L., Jager, M., Barreau, C., Chang, P., Guyader, H. L., Manuel, M., & Houliston, E. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.01.018 · Cited by 115 · see citing works
JAK–STAT is restrained by Notch to control cell proliferation of the Drosophila intestinal stem cells
Liu, W., Singh, S. R., & Hou, S. X. (2010) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22482 · Cited by 115 · see citing works
Feeding in a Calcareous Sponge: Particle Uptake by Pseudopodia
Leys, S. P., & Eerkes‐Medrano, D. (2006) · Biological Bulletin · doi:10.2307/4134590 · Cited by 112 · see citing works
Genetic redundancy in endoderm specification within the genus Caenorhabditis
Maduro, M., Hill, R. J., Heid, P. J., Newman-Smith, E. D., Zhu, J., Priess, J. R., & Rothman, J. H. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.05.016 · Cited by 110 · see citing works
Ultrastructure of the copper-accumulating region of the Drosophila larval midgut
Filshie, B. K., Poulson, D. F., & Waterhouse, D. F. (1971) · Tissue and Cell · doi:10.1016/s0040-8166(71)80033-2 · Cited by 108 · see citing works
β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii
Darras, S., Gerhart, J. C., Terasaki, M., Kirschner, M. W., & Lowe, C. J. (2011) · Development · doi:10.1242/dev.059493 · Cited by 106 · see citing works
Hepatocyte nuclear factor 1α and β control terminal differentiation and cell fate commitment in the gut epithelium
D'Angelo, A., Bluteau, O., García-González, M. Á., Gresh, L., Doyen, A., Garbay, S., Robine, S., & Pontoglio, M. (2010) · Development · doi:10.1242/dev.044420 · Cited by 105 · see citing works
Developmental expression of foxA and gata genes during gut formation in the polychaete annelid, Capitella sp. I
Boyle, M. J., & Seaver, E. C. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00216.x · Cited by 104 · see citing works
Depletion of the Colonic Epithelial Precursor Cell Compartment Upon Conditional Activation of the Hedgehog Pathway
van Dop, W. A., Uhmann, A., Wijgerde, M., Sleddens–Linkels, E., Heijmans, J., Offerhaus, G. J. A., Weerman, M. A. V. D. B., Boeckxstaens, G. E., Hommes, D. W., Hardwick, J. C. H., et al. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.02.068 · Cited by 103 · see citing works
Intestinal stem cells and epithelial–mesenchymal interactions in the crypt and stem cell niche
Shaker, A., & Rubin, D. C. (2010) · Translational research · doi:10.1016/j.trsl.2010.06.003 · Cited by 102 · see citing works
Basic helix‐loop‐helix transcription factors and enteroendocrine cell differentiation
Li, H. J., Ray, S. K., Singh, N. K., Johnston, B., & Leiter, A. B. (2011) · Diabetes Obesity and Metabolism · doi:10.1111/j.1463-1326.2011.01438.x · Cited by 96 · see citing works
Quiescent gastric stem cells maintain the adult Drosophila stomach
Strand, M., & Micchelli, C. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109794108 · Cited by 95 · see citing works
Neurogenin 3 and the enteroendocrine cell lineage in the adult mouse small intestinal epithelium
Bjerknes, M., & Cheng, H. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.07.040 · Cited by 90 · see citing works
Recent Insights into Cnidarian Phylogeny
Collins, A. G. (2009) · Smithsonian contributions to the marine sciences · doi:10.5479/si.01960768.38.139 · Cited by 88 · see citing works
Cell proliferation and early differentiation during embryonic development and metamorphosis ofHydractinia echinata
Plickert, G., Kroiher, M., & Munck, A. (1988) · Development · doi:10.1242/dev.103.4.795 · Cited by 87 · see citing works
β-Catenin is required for the establishment of vegetal embryonic fates in the nemertean, Cerebratulus lacteus
Henry, J. J., Perry, K. J., Wever, J., Seaver, E. C., & Martindale, M. Q. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.02.042 · Cited by 87 · see citing works
Regulation of Hematopoietic Stem Cells by the Niche
Arai, F., Hirao, A., & Suda, T. (2005) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2005.03.002 · Cited by 87 · see citing works
Regulation of mammalian neural development by helix-loop-helix transcription factors.
Kageyama, R., Sasai, Y., Akazawa, C., Ishibashi, M., Takebayashi, K., Shimizu, C., Tomita, K., & Nakanishi, S. (1995) · PubMed · Cited by 83 · see citing works
Delta1 Expression, Cell Cycle Exit, and Commitment to a Specific Secretory Fate Coincide within a Few Hours in the Mouse Intestinal Stem Cell System
Stamataki, D., Holder, M. V., Hodgetts, C., Jeffery, R. E., Nye, E. L., Spencer‐Dene, B., Winton, D. J., & Lewis, J. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024484 · Cited by 83 · see citing works
Development of the Drosophila entero-endocrine lineage and its specification by the Notch signaling pathway
Takashima, S., Adams, K. L., Ortiz, P. A., et al. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.01.039 · Cited by 81 · see citing works
Self-citation
Neurogenic and proneural genes control cell fate specification in the Drosophila endoderm
Tepaß, U., & Hartenstein, V. (1995) · Development · doi:10.1242/dev.121.2.393 · Cited by 81 · see citing works
Self-citation
The germ plasm component vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata
Rebscher, N., Volk, C., Teo, R., & Plickert, G. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21562 · Cited by 77 · see citing works
Role of the septate junction in the regulation of paracellular transepithelial flow.
Lord, B. A. P., & DiBona, D. R. (1976) · The Journal of Cell Biology · doi:10.1083/jcb.71.3.967 · Cited by 75 · see citing works
A forkhead gene related to HNF-3β is required for gastrulation and axis formation in the ascidian embryo
Olsen, C. L., & Jeffery, W. R. (1997) · Development · doi:10.1242/dev.124.18.3609 · Cited by 75 · see citing works
Afork head/HNF-3 Homolog Expressed in the Pharynx and Intestine of theCaenorhabditis elegansEmbryo
Azzaria, M., Goszczynski, B., Chung, M. A., Kalb, J. M., & McGhee, J. D. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0219 · Cited by 72 · see citing works
Migration and differentiation potential of stem cells in the cnidarian Hydractinia analysed in eGFP-transgenic animals and chimeras
Künzel, T., Heiermann, R., Uri Frank, A., Müller, W. D. A., Tilmann, W., Bause, M., Nonn, A., Helling, M., Schwarz, R. S., & Plickert, G. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.08.017 · Cited by 70 · see citing works
Gland cells arise by differentiation from interstitial cells in Hydra attenuata
Bode, H. R., Heimfeld, S., Chow, M. A., & Huang, L. W. (1987) · Developmental Biology · doi:10.1016/0012-1606(87)90321-6 · Cited by 70 · see citing works
Microanatomy of the cubopolyp,Tripedalia cystophora (Class Cubozoa)
Chapman, D. M. (1978) · Helgoländer Wissenschaftliche Meeresuntersuchungen · doi:10.1007/bf02296994 · Cited by 66 · see citing works
Endocytosis of latex beads by the exopinacoderm in the fresh water sponge Ephydatia fluviatilis: An in vitro and in situ study in SEM and TEM
Willenz, P., & Van de Vyver, G. (1982) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(82)90005-3 · Cited by 66 · see citing works
Notch signaling in intestinal homeostasis across species: the cases of Drosophila, Zebrafish and the mouse
Fré, S., Bardin, A. J., Robine, S., & Louvard, D. (2011) · Experimental Cell Research · doi:10.1016/j.yexcr.2011.06.012 · Cited by 64 · see citing works
Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula)
Boyle, M. J., & Seaver, E. C. (2010) · EvoDevo · doi:10.1186/2041-9139-1-2 · Cited by 64 · see citing works
Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa
Martín-Durán, J. M., & Romero, R. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.01.032 · Cited by 60 · see citing works
The Gene Regulatory Cascade Linking Proneural Specification with Differentiation in Drosophila Sensory Neurons
Cachero, S., Simpson, T. I., Lage, P. Z., Ma, L., Newton, F. G., Holohan, E. E., Armstrong, J. D., & Jarman, A. P. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000568 · Cited by 59 · see citing works
Placozoa and the evolution of Metazoa and intrasomatic cell differentiation
Schierwater, B., de Jong, D., & DeSalle, R. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.09.023 · Cited by 59 · see citing works
GATA factors as key regulatory molecules in the development of Drosophila endoderm
Murakami, R., Okumura, T., & Uchiyama, H. (2005) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2005.00836.x · Cited by 58 · see citing works
Drosophila Neural Stem Cells: Cell Cycle Control of Self-Renewal, Differentiation, and Termination in Brain Development
Reichert, H. (2011) · Results and problems in cell differentiation · doi:10.1007/978-3-642-19065-0_21 · Cited by 57 · see citing works
Gland cells in Hydra: Cell cycle kinetics and development
Schmidt, T., & David, C. N. (1986) · Journal of Cell Science · doi:10.1242/jcs.85.1.197 · Cited by 55 · see citing works
Transdifferentiation and regeneration in vitro
Schmid, V., Wydler, M. U., & Alder, H. (1982) · Developmental Biology · doi:10.1016/0012-1606(82)90193-2 · Cited by 50 · see citing works
Reduced Notch Signaling Leads to Renal Cysts and Papillary Microadenomas
Surendran, K., Selassie, M., Liapis, H., Krigman, H. R., & Kopan, R. (2010) · Journal of the American Society of Nephrology · doi:10.1681/asn.2009090925 · Cited by 48 · see citing works
The relationship of mucoid substances and ion and water transport, with new data on intestinal goblet cells and a model for gastric secretion.
Bl, G. (1989) · PubMed · Cited by 48 · see citing works
The fine structure of the planarianPolycelis tenuis (Iijima)
Bowen, I. D., & Ryder, T. A. (1974) · PROTOPLASMA · doi:10.1007/bf01276353 · Cited by 47 · see citing works
The fine structure of the planarianPolycelis tenuis Iijima
Bowen, I. D., Ryder, T. A., & Thompson, J. A. (1974) · PROTOPLASMA · doi:10.1007/bf02055779 · Cited by 47 · see citing works
The effects of starvation on the planarian worm Polycelis tenuis iijima
Bowen, I. D., Ryder, T. A., & Dark, C. (1976) · Cell and Tissue Research · doi:10.1007/bf00214208 · Cited by 46 · see citing works
Specific roles for the GATA transcription factors end-1 and end-3 during C. elegans E-lineage development
Boeck, M. E., Boyle, T., Bao, Z., et al. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.08.002 · Cited by 44 · see citing works
Gastrodermal structure and feeding responses in the scleractinian Mycetophyllia reesi, a coral with novel digestive filaments
Goldberg, W. M. (2002) · Tissue and Cell · doi:10.1016/s0040-8166(02)00008-3 · Cited by 43 · see citing works
The fine structure of the hypostome and mouth of hydra
Wood, R. L. (1979) · Cell and Tissue Research · doi:10.1007/bf00236142 · Cited by 42 · see citing works
Mechanisms of nutritive endocytosis i. phagocytic versatility and cellular recognition in Chlorohydra digestive cells, a scanning electron microscope study
McNeil, P. L. (1981) · Journal of Cell Science · doi:10.1242/jcs.49.1.311 · Cited by 42 · see citing works
Pattern of cell proliferation in embryogenesis and planula development ofHydractinia echinata predicts the postmetamorphic body pattern
Kroiher, M., Plickert, G., & Müller, W. A. (1990) · Development Genes and Evolution · doi:10.1007/bf01681488 · Cited by 36 · see citing works
Histological and ultrastructural studies of the basal disk of Hydra
Davis, L. (1975) · Cell and Tissue Research · doi:10.1007/bf00223266 · Cited by 34 · see citing works
Temporal differentiation and migration of substance P, serotonin, and secretin immunoreactive enteroendocrine cells in the mouse proximal small intestine
Aiken, K. D., & Roth, K. A. (1992) · Developmental Dynamics · doi:10.1002/aja.1001940406 · Cited by 30 · see citing works
Intestinal stem cell, muscular niche and Wingless signaling
Lin, G., & Xi, R. (2008) · Fly · doi:10.4161/fly.7428 · Cited by 29 · see citing works
Hydra regeneration from recombined ectodermal and endodermal tissueII. Differential stability in the ectodermal and endodermal epithelial organization
Murate, M., Kishimoto, Y., Sugiyama, T., et al. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.16.1919 · Cited by 29 · see citing works
Conserved genetic pathways controlling the development of the diffuse endocrine system in vertebrates and Drosophila
Hartenstein, V., Takashima, S., & Adams, K. L. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2009.12.002 · Cited by 24 · see citing works
Self-citation
The conserved role and divergent regulation of foxa, a pan-eumetazoan developmental regulatory gene
de‐Leon, S. B. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.11.027 · Cited by 22 · see citing works
Multifunctional features of a gastrodermal sensory cell inHydra: three-dimensional study
Westfall, J. A., Wilson, J. D., Rogers, R. A., & Kinnamon, J. C. (1991) · Journal of Neurocytology · doi:10.1007/bf01235543 · Cited by 19 · see citing works
Migration of I-cells from ectoderm to endoderm in Hydra attenuata Pall (Cnidaria, Hydrozoa) and their subsequent differentiation
Smid, I., & Tardent, P. (1984) · Developmental Biology · doi:10.1016/0012-1606(84)90246-x · Cited by 19 · see citing works
Ultrastructure of the digestive tract ofGyliauchen nahaensis (Platyhelminthes, Digenea), an inhabitant of the hindgut of herbivorous fishes
Jones, M. K., Hughes-Stamm, S. R., East, R. M., et al. (2000) · Journal of Morphology · doi:10.1002/1097-4687(200012)246:3 · Cited by 19 · see citing works
The Emergence of Pattern in Embryogenesis: Regulation of β-Catenin Localization During Early Sea Urchin Development
Ettensohn, C. A. (2006) · Science s STKE · doi:10.1126/stke.3612006pe48 · Cited by 18 · see citing works
Thyroid hormone-regulated expression of nuclear lamins correlates with dedifferentiation of intestinal epithelial cells during Xenopus laevis metamorphosis
Hasebe, T., Kajita, M., Iwabuchi, M., et al. (2011) · Development Genes and Evolution · doi:10.1007/s00427-011-0371-7 · Cited by 13 · see citing works
Junctional types in the tissues of an onychophoran: The apparent lack of gap and tight junctions in Peripatus
Lane, N. J., Campiglia, S. S., & Lee, W. M. (1994) · Tissue and Cell · doi:10.1016/0040-8166(94)90090-6 · Cited by 12 · see citing works
Intercellular junctions in the hepatopancreas of the lobster Nephrops norvegicus
Lane, N. J., Harrison, J. B., & Lee, W. M. (1985) · Biology of the Cell · doi:10.1111/j.1768-322x.1985.tb00346.x · Cited by 11 · see citing works
The Cell Cycle Machinery and Asymmetric Cell Division of Neural Progenitors in the Drosophila Embryonic Central Nervous System
Chia, W. N., Cai, Y., Morin, X., et al. (2001) · Novartis Foundation symposium · doi:10.1002/0470846666.ch11 · Cited by 9 · see citing works
Characterization of Cer-1 cis-regulatory region during early Xenopus development
Silva, A. C., Filipe, M., Steinbeißer, H., & Belo, J. A. (2011) · Development Genes and Evolution · doi:10.1007/s00427-011-0357-5 · Cited by 4 · see citing works

Flagged first, then by citations

Research works printed but not linked: 11

Chia FS Koss R 1994 Asteroidea Microscopic Anatomy of Invertebrates Harrison FW Chia TS 14 Wiley Liss New York 169 246
Coons LB Alberti G 1999 Acari: Ticks Microscopic Anatomy of Invertebrates Harrison FW Foelix AF 8B Wiley Liss New York 267 514
Hernandez-Nicaise ML 1991 Ctenophora Microscopic Anatomy of Invertebrates Harrison FW Westfall JA 2 Wiley Liss New York 359 418
Icely JD Nott JAR 1992 Digestion and absorption: digestive system and associated organs Microscopic Anatomy of Invertebrates Harrison FW Humes AG 10 Wiley Liss New York 147 201
Mukai H Terakado K Reed CG 1997 Bryozoa Microscopic Anatomy of Invertebrates Harrison FW Woolacott RM 13 Wiley Liss New York 45 206
Nielsen C Jespersen A 1997 Entoprocta Microscopic Anatomy of Invertebrates Harrison FW Woollacott RM 14 Wiley Liss New York 13 44
Rice ME 1993 Sipuncula Microscopic Anatomy of Invertebrates Harrison FW Rice ME 12 Wiley Liss New York 237 326
Rieger R 1991 Turbellaria Microscopic Anatomy of Invertebrates Harrison FW Bogitsh J 2 Wiley Liss New York 1 140
Ruppert EE 1997 Cephalochordata (Acrania) Microscopic Anatomy of Invertebrates Harrison FW Ruppert EE 15 Wiley Liss New York 349 504
Turbeville JM 1991 Nmertinea Microscopic Anatomy of Invertebrates Harrison FW Bogitsh 3 Wiley Liss New York 285 328
Wright KA 1991 Nematoda Microscopic Anatomy of Invertebrates Harrison FW Ruppert EE 4 Wiley Liss New York 111 195

Sorted by citations

Profiling cellular diversity in sponges informs animal cell type and nervous system evolution
Musser, J. M., Schippers, K. J., Nickel, M., Mizzon, G., Kohn, A. B., Pape, C., Ronchi, P., Papadopoulos, N., Tarashansky, A. J., Hammel, J. U., et al. (2021) · Science · doi:10.1126/science.abj2949 · Cited by 242 · see citing works
Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution
Arendt, D., Benito-Gutierrez, E., Brunet, T., & Marlow, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0286 · Cited by 112 · see citing works
A non-bilaterian perspective on the development and evolution of animal digestive systems
Steinmetz, P. R. H. (2019) · Cell and Tissue Research · doi:10.1007/s00441-019-03075-x · Cited by 67 · see citing works

Comparison of bacterial communities between midgut and midgut contents in two silkworms, Antheraea pernyi and Bombyx mori
Wang, H., Zhang, J., Wang, X., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-69906-y · Cited by 20 · see citing works
Spatial distribution of orally administered viral fusolin protein in the insect midgut and possible synergism between fusolin and digestive proteases to disrupt the midgut peritrophic matrix
Mitsuhashi, W., Shimura, S., Miyamoto, K., et al. (2018) · Archives of Virology · doi:10.1007/s00705-018-4013-5 · Cited by 7 · see citing works
On the Hydrogen-Ion Concentration in the Alimentary Canal of Certain Orthopteroid Insects.
Srivastava, U. S., & Srivastava, P. D. (2017) · Universitätsbibliothek JCS Frankfurt · doi:10.21248/contrib.entomol.6.5-6.493-498 · Cited by 4 · see citing works
Cellulolytic environment in the midgut of the wood-feeding higher termite Nasutitermes takasagoensis
Tokuda, G., Watanabe, H., Hojo, M., et al. (2011) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2011.10.012 · Cited by 42 · see citing works
Histoarchitectural alteration in midgut of Dysdercus koenigii (Fabricius) (Hemiptera: Pyrrhocoridae) treated with chlorpyrifos
Laiba, Amir, M., Yasmeen, S., et al. (2021) · Journal of Entomology and Zoology Studies

Authors: Takashima, S., Gold, D., & Hartenstein, V.
Affiliations: University of California, Los Angeles (US)
Corresponding author: Hartenstein, Volker
ORCID: Takashima, Shigeo
Gold, David
Hartenstein, Volker
Venue: Development Genes and Evolution
Publisher: Springer Science and Business Media LLC
Published: 2012-11-21
Volume: 223
Issue: 1-2
Pages: 85-102
ISSN: 0043-5546 (ISSN-L)
0949-944X
1432-041X
DOI: 10.1007/s00427-012-0422-8
PMC: PMC3873164
OpenAlex: W2118177287
Cited by: 67
References: 136
Citations by year: 2025: 1 · 2024: 2 · 2023: 5 · 2022: 2 · 2021: 4 · 2020: 3 · 2019: 12 · 2018: 5 · 2017: 9 · 2016: 4 · 2015: 9 · 2014: 3 · 2013: 7 · 2012: 1
FWCI: 0.58
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Development Genes and Evolution (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Human Genome Research Institute (T32HG002536)
National Institute of General Medical Sciences (NIH/1 R01GM087373, R01GM087373)
National Institute of Neurological Disorders and Stroke (R01NS054814)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Digestive system and related health
Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Keywords: intestinal stem cells, midgut, intestinal regeneration, neoblasts, Platyhelminthes, enterocytes, endocrine cells, gland cells, stem cell proliferation, comparative development
MeSH terms: Animals, Biological Evolution, Humans, Intestines, Stem Cells, Vertebrates, Signal Transduction, Enteroendocrine Cells, Enterocytes, Stem Cell Niche

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

Stem cells and lineages of the intestine: a developmental and evolutionary perspective

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks