Skip to main content
Log in

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

  • Review
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aiken KD, Roth KA (1992) Temporal differentiation and migration of substance P, serotonin, and secretin immunoreactive enteroendocrine cells in the mouse proximal small intestine. Dev Dyn 194:303–310

    Article  PubMed  CAS  Google Scholar 

  • Ang SL, Wierda A, Wong D, Stevens KA, Cascio S, Rossant J, Zaret KS (1993) The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119(4):1301–1315

    PubMed  CAS  Google Scholar 

  • Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118(2):149–161

    Article  PubMed  CAS  Google Scholar 

  • Arai F, Hirao A, Suda T (2005) Regulation of hematopoietic stem cells by the niche. Trends Cardiovasc Med 15(2):75–79

    Article  PubMed  CAS  Google Scholar 

  • Azzaria M, Goszczynski B, Chung MA, Kalb JM, McGhee JD (1996) A fork head/HNF-3 homolog expressed in the pharynx and intestine of the Caenorhabditis elegans embryo. Dev Biol 178(2):289–303

    Article  PubMed  CAS  Google Scholar 

  • Baguñà J (2012) The planarian neoblast: the rambling history of its origin and some current black boxes. Int J Dev Biol 56(1–3):19–37

    Article  PubMed  CAS  Google Scholar 

  • Bardin AJ, Perdigoto CN, Southall TD, Brand AH, Schweisguth F (2010) Transcriptional control of stem cell maintenance in the Drosophila intestine. Development 137(5):705–714

    Article  PubMed  CAS  Google Scholar 

  • Bei Y, Hogan J, Berkowitz LA, Soto M, Rocheleau CE, Pang KM, Collins J, Mello CC (2002) SRC-1 and Wnt signaling act together to specify endoderm and to control cleavage orientation in early C. elegans embryos. Dev Cell 3(1):113–125

    Article  PubMed  CAS  Google Scholar 

  • Bjerknes M, Cheng H (2006) Neurogenin 3 and the enteroendocrine cell lineage in the adult mouse small intestinal epithelium. Dev Biol 300:722–735

    Article  PubMed  CAS  Google Scholar 

  • Bode HR, Heimfeld S, Chow MA, Huang LW (1987) Gland cells arise by differentiation from interstitial cells in Hydra attenuata. Dev Biol 122(2):577–585

    Article  PubMed  CAS  Google Scholar 

  • Boeck ME, Boyle T, Bao Z, Murray J, Mericle B, Waterston R (2011) Specific roles for the GATA transcription factors end-1 and end-3 during C. elegans E-lineage development. Dev Biol 358(2):345–355

    Article  PubMed  CAS  Google Scholar 

  • Bossard P, Zaret KS (1998) GATA transcription factors as potentiators of gut endoderm differentiation. Development 125(24):4909–4917

    PubMed  CAS  Google Scholar 

  • Bowen ED, Ryder TA, Thompson JA (1974) The fine structure of the planarian Polycelis tenuis Iijima. II. The intestine and gastrodermal phagocytosis. Protoplasma 79:1–17

    Article  PubMed  CAS  Google Scholar 

  • Bowen ED, Ryder TA, Dark C (1976) The effects of starvation on the planarian worm Polycelis tenuis Iijima. Cell Tissue Res 169(2):193–209

    Article  PubMed  CAS  Google Scholar 

  • Bowman SK, Rolland V, Betschinger J, Kinsey KA, Emery G, Knoblich JA (2008) The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev Cell 14(4):535–546

    Article  PubMed  CAS  Google Scholar 

  • Boyle MJ, Seaver EC (2008) Developmental expression of foxA and gata genes during gut formation in the polychaete annelid, Capitella sp. I. Evol Dev 10:89–105

    Article  PubMed  CAS  Google Scholar 

  • Boyle MJ, Seaver EC (2010) Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula). EvoDevo 1:2

    Article  PubMed  CAS  Google Scholar 

  • Cachero S, Simpson TI, Zur Lage PI, Ma L, Newton FG, Holohan EE, Armstrong JD, Jarman AP (2011) The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons. PLoS Biol 9(1):e1000568

    Article  PubMed  CAS  Google Scholar 

  • Campos-Ortega JA (1995) Genetic mechanisms of early neurogenesis in Drosophila melanogaster. Mol Neurobiol 10(2–3):75–89

    Article  PubMed  CAS  Google Scholar 

  • Campuzano S, Modolell J (1992) Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet 8:202–208

    PubMed  CAS  Google Scholar 

  • Chapman DM (1978) Microanatomy of the cubopolyp, Tripedalia cystophora (Class Cubozoa). Helgoländer wiss Meeresunters 31:128–168

    Article  Google Scholar 

  • Chia FS, Koss R (1991). Asteroidea. In: Harrison FW, Chia TS (eds). Microscopic anatomy of invertebrates vol. 14. Wiley: New York, pp169–246

  • Chia W, Cai Y, Morin X, Tio M, Udolph G, Yu F, Yang X (2001) The cell cycle machinery and asymmetric cell division of neural progenitors in the Drosophila embryonic central nervous system. Novartis Found Symp 237:139–15

    Article  PubMed  CAS  Google Scholar 

  • Cioffi M (1979) The morphology and fine structure of the larval midgut of a moth (Manduca sexta) in relation to active ion transport. Tissue Cell 11(3):467–479

    Article  PubMed  CAS  Google Scholar 

  • Collins AG (2009) Recent insights into cnidarian phylogeny. Smithsonian Contrib Mar Sci 38:139–149

    Google Scholar 

  • Coons LB, Alberti G (1999). Acari: ticks. In: Harrison FW, Foelix AF (eds). Microscopic anatomy of invertebrates vol. 8B. Wiley: New York, pp 267–514

  • Crosnier C, Vargesson N, Gschmeissner S, Ariza-McNaughton L, Morrison A, Lewis J (2005) Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132:1093–1104

    Article  PubMed  CAS  Google Scholar 

  • Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 7:349–359

    Article  PubMed  CAS  Google Scholar 

  • D'Angelo A, Bluteau O, Garcia-Gonzalez MA, Gresh L, Doyen A, Garbay S, Robine S, Pontoglio M (2010) Hepatocyte nuclear factor 1alpha and beta control terminal differentiation and cell fate commitment in the gut epithelium. Development 137(9):1573–1582

    Article  PubMed  CAS  Google Scholar 

  • Darras S, Gerhart J, Terasaki M, Kirschner M, Lowe CJ (2011) β-catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii. Development 138(5):959–970

    Article  PubMed  CAS  Google Scholar 

  • David CN, Campbell RD (1972) Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. J Cell Sci 11(2):557–568

    PubMed  CAS  Google Scholar 

  • David CN, Gierer A (1974) Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. J Cell Sci 16(2):359–375

    PubMed  CAS  Google Scholar 

  • Davis LE (1975) Histological and ultrastructural studies of the basal disk of Hydra. III. The gastrodermis and the mesoglea. Cell Tissue Res 162(1):107–118

    Article  PubMed  CAS  Google Scholar 

  • de Leon SB (2011) The conserved role and divergent regulation of foxa, a pan-eumetazoan developmental regulatory gene. Dev Biol 357(1):21–26

    Article  CAS  Google Scholar 

  • de Navascués J, Perdigoto CN, Bian Y, Schneider MH, Bardin AJ, Martínez-Arias A, Simons BD (2012) Drosophila midgut homeostasis involves neutral competition between symmetrically dividing intestinal stem cells. EMBO J 31(11):2473–2485

    Article  PubMed  CAS  Google Scholar 

  • Dubreuil RR (2004) Copper cells and stomach acid secretion in the Drosophila midgut. Int J Biochem Cell Biol 36(5):745–752

    Article  PubMed  CAS  Google Scholar 

  • Ettensohn CA (2006) The emergence of pattern in embryogenesis: regulation of beta-catenin localization during early sea urchin development. Sci STKE 2006(361):e48

    Article  Google Scholar 

  • Fevr T, Robine S, Louvard D, Huelsken J (2007) Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol Cell Biol 27(21):7551–7559

    Article  PubMed  CAS  Google Scholar 

  • Filshie BK, Poulson DF, Waterhouse DF (1971) Ultrastructure of the copper-accumulating region of the Drosophila larval midgut. Tissue Cell 3(1):77–102

    Article  PubMed  CAS  Google Scholar 

  • Forsthoefel DJ, Park AE, Newmark PA (2011) Stem cell-based growth, regeneration, and remodeling of the planarian intestine. Dev Biol 356(2):445–459

    Article  PubMed  CAS  Google Scholar 

  • Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, Artavanis-Tsakonas S (2005) Notch signals control the fate of immature progenitor cells in the intestine. Nature 435(7044):964–968

    Article  PubMed  CAS  Google Scholar 

  • Fre S, Hannezo E, Sale S, Huyghe M, Lafkas D, Kissel H, Louvi A, Greve J, Louvard D, Artavanis-Tsakonas S (2011a) Notch lineages and activity in intestinal stem cells determined by a new set of knock-in mice. PLoS One 6(10):e25785

    Article  PubMed  CAS  Google Scholar 

  • Fre S, Bardin A, Robine S, Louvard D (2011b) Notch signaling in intestinal homeostasis across species: the cases of Drosophila, zebrafish and the mouse. Exp Cell Res 317(19):2740–2747

    Article  PubMed  CAS  Google Scholar 

  • Goldberg WM (2002) Gastrodermal structure and feeding responses in the scleractinian Mycetophyllia reesi, a coral with novel digestive filaments. Tissue Cell 34(4):246–261

    Article  PubMed  Google Scholar 

  • Grell KG, Ruthmann A (1991). Placozoa. Harrison FW, Westfall JA (eds). In: Microscopic anatomy of invertebrates vol. 2. Wiley: New York, pp 13–28.

  • Guillemot F (1999) Vertebrate bHLH genes and the determination of neuronal fates. Exp Cell Res 253:357–364

    Article  PubMed  CAS  Google Scholar 

  • Gupta BL (1989) The relationship of mucoid substances and ion and water transport, with new data on intestinal goblet cells and a model for gastric secretion. Symp Soc Exp Biol 43:81–110

    PubMed  CAS  Google Scholar 

  • Haegebarth A, Clevers H (2009) Wnt signaling, lgr5, and stem cells in the intestine and skin. Am J Pathol 174(3):715–721

    Article  PubMed  CAS  Google Scholar 

  • Hartenstein V, Takashima S, Adams KL (2010) Conserved genetic pathways controlling the development of the diffuse endocrine system in vertebrates and Drosophila. Gen Comp Endocrinol 166(3):462–469

    Article  PubMed  CAS  Google Scholar 

  • Hasebe T, Kajita M, Iwabuchi M, Ohsumi K, Ishizuya-Oka A (2001) Thyroid hormone-regulated expression of nuclear lamins correlates with dedifferentiation of intestinal epithelial cells during Xenopus laevis metamorphosis. Dev Genes Evol 221:199–208

    Article  CAS  Google Scholar 

  • Henning SJ, Rubin DC, Shulman R (1994) Ontogeny of the intestinal mucosa. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven, New York, pp 571–610

    Google Scholar 

  • Henry JQ, Perry KJ, Wever J, Seaver E, Martindale MQ (2008) Beta-catenin is required for the establishment of vegetal embryonic fates in the nemertean, Cerebratulus lacteus. Dev Biol 317(1):368–379

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Nicaise ML (1991) Ctenophora. In: Harrison FW, Westfall JA (eds). Microscopic anatomy of invertebrates vol. 2. Wiley: New York, pp 359–418

  • Icely JD, Nott JA R (1992) Digestion and absorption: digestive system and associated organs. In: Harrison FW, Humes AG (eds). Microscopic anatomy of invertebrates, vol. 10. Wiley: New York, pp 147–201

  • Jacquemin P, Durviaux SM, Jensen J, Godfraind C, Gradwohl G, Guillemot F, Madsen OD, Carmeliet P, Dewerchin M, Collen D, Rousseau GG, Lemaigre FP (2000) Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Mol Cell Biol 20(12):4445–4454

    Article  PubMed  CAS  Google Scholar 

  • Jenny M, Uhl C, Roche C, Duluc I, Guillermin V, Guillemot F, Jensen J, Kedinger M, Gradwohl G (2002) Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium. EMBO J 21:6338–6347

    Article  PubMed  CAS  Google Scholar 

  • Jensen J, Pedersen EE, Galante P, Hald J, Heller RS, Ishibashi M, Kageyama R, Guillemot F, Serup P, Madsen OD (2000) Control of endodermal endocrine development by Hes-1. Nat Genet 24:36–44

    Article  PubMed  CAS  Google Scholar 

  • Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA (2009) Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137(7):1343–1355

    Article  PubMed  Google Scholar 

  • Jiang H, Grenley MO, Bravo MJ, Blumhagen RZ, Edgar BA (2011) EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell 8(1):84–95

    Article  PubMed  CAS  Google Scholar 

  • Jones MK, Hughes-Stamm SR, East RM, Cribb TH (2000) Ultrastructure of the digestive tract of Gyliauchen nahaensis (Platyhelminthes, Digenea), an inhabitant of the hindgut of herbivorous fishes. J Morphol 246(3):198–211

    Article  PubMed  CAS  Google Scholar 

  • Kageyama R, Sasai Y, Akazawa C, Ishibashi M, Takebayashi K, Shimizu C, Tomita K, Nakanishi S (1995) Regulation of mammalian neural development by helix-loop-helix transcription factors. Crit Rev Neurobiol 9:177–188

    PubMed  CAS  Google Scholar 

  • Karpowicz P, Perez J, Perrimon N (2010) The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137(24):4135–4145

    Article  PubMed  CAS  Google Scholar 

  • Kroiher M, Plickert G, Müller WA (1990) Pattern of cell proliferation in embryogenesis and planula development of Hydractinia echinata predicts the postmetamorphic body pattern. Roux's Arch Dev Biol 199(3):156–163

    Article  Google Scholar 

  • Künzel T, Heiermann R, Frank U, Müller W, Tilmann W, Bause M, Nonn A, Helling M, Schwarz RS, Plickert G (2010) Migration and differentiation potential of stem cells in the cnidarian Hydractinia analysed in eGFP-transgenic animals and chimeras. Dev Biol 348(1):120–129

    Article  PubMed  CAS  Google Scholar 

  • Lane NJ, Harrison JB, Lee WM (1984) Intercellular junctions in the hepatopancreas of the lobster Nephrops norvegicus. Biol Cell 52(3):267–277

    Article  PubMed  CAS  Google Scholar 

  • Lane NJ, Campiglia SS, Lee WM (1994) Junctional types in the tissue of an onychophoran: the apparent lack of gap and tight junctions in Perpatus. Tissue Cell 26(1):143–154

    Google Scholar 

  • Leclère L, Jager M, Barreau C, Chang P, Le Guyader H, Manuel M, Houliston E (2012) Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia. Dev Biol 364(2):236–248

    Article  PubMed  CAS  Google Scholar 

  • Lee CS, Perreault N, Brestelli JE, Kaestner KH (2002) Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev 16:1488–1497

    Article  PubMed  CAS  Google Scholar 

  • Lee PN, Kumburegama S, Marlow HQ, Martindale MQ, Wikramanayake AH (2007) Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. Dev Biol 310(1):169–186

    Article  PubMed  CAS  Google Scholar 

  • Lee WC, Beebe K, Sudmeier L, Micchelli CA (2009) Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation. Development 136(13):2255–2264

    Article  PubMed  CAS  Google Scholar 

  • Lehane MJ (1998) The midgut. In: Harrison FW, Locke M (eds) Microscopic anatomy of invertebrates. Wiley, New York, pp 725–746

    Google Scholar 

  • Leys SP, Eerkes-Medrano DI (2006) Feeding in a calcareous sponge: particle uptake by pseudopodia. Biol Bull 211(2):157–171

    Article  PubMed  Google Scholar 

  • Li HJ, Ray SK, Singh NK, Johnston B, Leiter AB (2011) Basic helix-loop-helix transcription factors and enteroendocrine cell differentiation. Diabetes Obes Metab 13(Suppl 1):5–12

    Article  PubMed  CAS  Google Scholar 

  • Li L, Clevers H (2010) Coexistence of quiescent and active adult stem cells in mammals. Science 327(5965):542–545

    Article  PubMed  CAS  Google Scholar 

  • Lin G, Xu N, Xi R (2008) Paracrine wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 455(7216):1119–1123

    Article  PubMed  CAS  Google Scholar 

  • Liu W, Singh SR, Hou SX (2010) JAK-STAT is restrained by Notch to control cell proliferation of the Drosophila intestinal stem cells. J Cell Biochem 109(5):992–999

    PubMed  CAS  Google Scholar 

  • Lo L, Dormand E, Greenwood A, Anderson DJ (2002) Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalian achaete-scute and atonal homologs in cultured neural progenitor cells. Development 129:1553–1567

    PubMed  CAS  Google Scholar 

  • Lord BA, DiBona DR (1976) Role of the septate junction in the regulation of paracellular transepithelial flow. J Cell Biol 71(3):967–972

    Article  PubMed  CAS  Google Scholar 

  • Maduro MF, Hill RJ, Heid PJ, Newman-Smith ED, Zhu J, Priess JR, Rothman JH (2005) Genetic redundancy in endoderm specification within the genus Caenorhabditis. Dev Biol 284(2):509–522

    Article  PubMed  CAS  Google Scholar 

  • Martín-Durán JM, Romero R (2011) Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa. Dev Biol 352:164–176

    Article  PubMed  CAS  Google Scholar 

  • Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131:2463–2474

    Article  PubMed  CAS  Google Scholar 

  • McLin VA, Henning SJ, Jamrich M (2009) The role of the visceral mesoderm in the development of the gastrointestinal tract. Gastroenterology 136(7):2074–2091

    Article  PubMed  CAS  Google Scholar 

  • McNeil PL (1981) Mechanisms of nutritive endocytosis. I. Phagocytic versatility and cellular recognition in Chlorohydra digestive cells, a scanning electron microscope study. J Cell Sci 49:311–339

    PubMed  CAS  Google Scholar 

  • Micchelli CA, Perrimon N (2006) Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439(7075):475–479

    Article  PubMed  CAS  Google Scholar 

  • Miller SJ, Lavker RM, Sun TT (2005) Interpreting epithelial cancer biology in the context of stem cells: tumor properties and therapeutic implications. Biochim Biophys Acta 1756:25–52

    PubMed  CAS  Google Scholar 

  • Müller WA, Teo R, Frank U (2004) Totipotent migratory stem cells in a hydroid. Dev Biol 275(1):215–224

    Article  PubMed  CAS  Google Scholar 

  • Mukai H, Terakado K, Reed CG (1997). Bryozoa. In: Harrison FW, Woolacott RM (eds). Microscopic anatomy of invertebrates, vol. 13. Wiley: New York, pp 45–206

  • Murakami R, Okumura T, Uchiyama H (2005) GATA factors as key regulatory molecules in the development of Drosophila endoderm. Dev Growth Differ 47(9):581–589

    Article  PubMed  CAS  Google Scholar 

  • Murate M, Kishimoto Y, Sugiyama T, Fujisawa T, Takahashi-Iwanaga H, Iwanaga T (1997) Hydra regeneration from recombined ectodermal and endodermal tissue. II. Differential stability in the ectodermal and endodermal epithelial organization. J Cell Sci 110(Pt 16):1919–1934

    PubMed  CAS  Google Scholar 

  • Nakanishi N, Renfer E, Technau U, Rentzsch F (2012) Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 139(2):347–357

    Article  PubMed  CAS  Google Scholar 

  • Nielsen C, Jespersen A (1997) Entoprocta. In: Harrison FW, Woollacott RM (eds). Microscopic anatomy of invertebrates, vol. 14. Wiley: New York, pp 13–44

  • Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470–474

    Article  PubMed  CAS  Google Scholar 

  • Ohlstein B, Spradling A (2007) Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential Notch signaling. Science 315:988–992

    Article  PubMed  CAS  Google Scholar 

  • Oliveri P, Walton KD, Davidson EH, McClay DR (2006) Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 133(21):4173–4181

    Article  PubMed  CAS  Google Scholar 

  • Olsen CL, Jeffery WR (1997) A forkhead gene related to HNF-3beta is required for gastrulation and axis formation in the ascidian embryo. Development 124(18):3609–3619

    PubMed  CAS  Google Scholar 

  • Plickert G, Kroiher M, Munck A (1988) Cell proliferation and early differentiation during embryonic development and metamorphosis of Hydractinia echinata. Development 103(4):795–803

    PubMed  CAS  Google Scholar 

  • Powell DW, Pinchuk IV, Saada JI, Chen X, Mifflin RC (2011) Mesenchymal cells of the intestinal lamina propria. Annu Rev Physiol 73:213–237

    Article  PubMed  CAS  Google Scholar 

  • Quyin AJ, Appleton PL, Carey FA, Steele RFC, Barker N, Clevers H, Ridgway RA, Sansom OJ, Näthke IS (2010) Spindle orientation bias in gut epithelial stem cell compartments. Cell Stem Cell 6:175–181

    Article  CAS  Google Scholar 

  • Rebscher N, Volk C, Teo R, Plickert G (2008) The germ plasm component Vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata. Dev Dyn 237(6):1736–1745

    Article  PubMed  CAS  Google Scholar 

  • Reichert H (2011) Drosophila neural stem cells: cell cycle control of self-renewal, differentiation, and termination in brain development. Results Probl Cell Differ 53:529–546

    Article  PubMed  CAS  Google Scholar 

  • Ren F, Wang B, Yue T, Yun EY, Ip YT, Jiang J (2010) Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc Natl Acad Sci U S A 107(49):21064–210649

    Article  PubMed  CAS  Google Scholar 

  • Rice ME (1993) Sipuncula. In: Harrison FW, Rice ME (eds). Microscopic anatomy of invertebrates vol. 12. Wiley: New York, pp 237–326

  • Rieger R (1991) Turbellaria. In: Harrison FW, Bogitsh J (eds). Microscopic anatomy of invertebrates, vol. 2. Wiley: New York, pp 1–140

  • Ruppert EE (1997) Cephalochordata (Acrania). In: Harrison FW, Ruppert EE (eds). Microscopic anatomy of invertebrates vol. 15. Wiley: New York, pp 349–504

  • Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469(7330):415–418

    Article  PubMed  CAS  Google Scholar 

  • Schierwater B, de Jong D, Desalle R (2009) Placozoa and the evolution of Metazoa and intrasomatic cell differentiation. Int J Biochem Cell Biol 41(2):370–379

    Article  PubMed  CAS  Google Scholar 

  • Schmid V, Wydler M, Alder H (1982) Transdifferentiation and regeneration in vitro. Dev Biol 92(2):476–488

    Article  PubMed  CAS  Google Scholar 

  • Schmidt T, David CN (1986) Gland cells in Hydra: cell cycle kinetics and development. J Cell Sci 85:197–215

    PubMed  CAS  Google Scholar 

  • Schonhoff SE, Giel-Moloney M, Leiter AB (2004) Development and differentiation of gut endocrine cells. Endocrinology 145:2639–2644

    Article  PubMed  CAS  Google Scholar 

  • Scoville DH, Sato T, He XC, Li L (2008) Current view: intestinal stem cells and signaling. Gastroenterology 134(3):849–864

    Article  PubMed  CAS  Google Scholar 

  • Seipel K, Yanze N, Schmid V (2004) The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int J Dev Biol 48(1):1–7

    Article  PubMed  CAS  Google Scholar 

  • Shaker A, Rubin DC (2010) Intestinal stem cells and epithelial–mesenchymal interactions in the crypt and stem cell niche. Transl Res 156(3):180–187

    Article  PubMed  CAS  Google Scholar 

  • Shaw RL, Kohlmaier A, Polesello C, Veelken C, Edgar BA, Tapon N (2010) The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137(24):4147–4158

    Article  PubMed  CAS  Google Scholar 

  • Shibata N, Rouhana L, Agata K (2010) Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians. Dev Growth Differ 52(1):27–41

    Article  PubMed  CAS  Google Scholar 

  • Silva AC, Filipe M, Steinbeisser H, Belo JA (2011) Characterization of Cer-1 cis-regulatory region during early Xenopus development. Dev Genes Evol 221:29–41

    Article  PubMed  CAS  Google Scholar 

  • Smid I, Tardent P (1984) Migration of I-cells from ectoderm to endoderm in Hydra attenuata Pall (Cnidaria, Hydrozoa) and their subsequent differentiation. Dev Biol 106(2):469–477

    Article  PubMed  CAS  Google Scholar 

  • Stamataki D, Holder M, Hodgetts C, Jeffery R, Nye E, Spencer-Dene B, Winton DJ, Lewis J (2011) Delta1 expression, cell cycle exit, and commitment to a specific secretory fate coincide within a few hours in the mouse intestinal stem cell system. PLoS One 6(9):e24484

    Article  PubMed  CAS  Google Scholar 

  • Strand M, Micchelli CA (2011) Quiescent gastric stem cells maintain the adult Drosophila stomach. Proc Natl Acad Sci U S A 108(43):17696–17701

    Article  PubMed  CAS  Google Scholar 

  • Surendran K, Selassie M, Liapis H, Krigman H, Kopan R (2010) Reduced Notch signaling leads to renal cysts and papillary microadenomas. J Am Soc Nephrol 21(5):819–832

    Article  PubMed  CAS  Google Scholar 

  • Takashima S, Adams KL, Ortiz PA, Ying CT, Moridzadeh R, Younossi-Hartenstein A, Hartenstein V (2011) Development of the Drosophila entero-endocrine lineage and its specification by the Notch signaling pathway. Dev Biol 353(2):161–172

    Article  PubMed  CAS  Google Scholar 

  • Tepass U, Hartenstein V (1994) The development of cellular junctions in the Drosophila embryo. Dev Biol 161(2):563–596

    Article  PubMed  CAS  Google Scholar 

  • Tepass U, Hartenstein V (1995) Neurogenic and proneural genes control the specification of non-neuronal cell types in the Drosophila endoderm. Development 121:393–405

    PubMed  CAS  Google Scholar 

  • Turbeville JM (1991) Nmertinea. In: Harrison FW, Bogitsh (eds). Microscopic anatomy of invertebrates vol. 3. Wiley: New York, pp 285–328

  • Van Dop WA, Uhmann A, Wijgerde M, Sleddens-Likels A, Heijmans J, Offerhaus GJ, van den Beergh Weerman MA, Boeckxstaens GE, Hommes DW, Hardwick JC, Hahn H, van den Brink GR (2009) Depletion of the colonic epithelial precursor cell compartment upon conditional activation of the Hedgehog pathway. Gastroenterology 136:2195–2203

    Article  PubMed  CAS  Google Scholar 

  • van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, Clevers H (2005) Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435:959–963

    Article  PubMed  CAS  Google Scholar 

  • Veenstra JA, Agricola HJ, Sellami A (2008) Regulatory peptides in fruit fly midgut. Cell Tissue Res 334:499–516

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Cortina G, Wu SV, Tran R, Cho JH, Tsai MJ, Bailey TJ, Jamrich M, Ament ME, Treem WR, Hill ID, Vargas JH, Gershman G, Farmer DG, Reyen L, Martín MG (2006) Mutant neurogenin-3 in congenital malabsorptive diarrhea. N Engl J Med 355(3):270–280

    Article  PubMed  CAS  Google Scholar 

  • Weber H, Symes CE, Walmsley ME, Rodaway AR, Patient RK (2000) A role for GATA5 in Xenopus endoderm specification. Development 127(20):4345–4360

    PubMed  CAS  Google Scholar 

  • Weigel D, Jürgens G, Küttner F, Seifert E, Jäckle H (1989) The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57(4):645–658

    Article  PubMed  CAS  Google Scholar 

  • Westfall JA, Wilson JD, Rogers RA, Kinnamon JC (1991) Multifunctional features of a gastrodermal sensory cell in Hydra: three-dimensional study. J Neurocytol 20(4):251–261

    Article  PubMed  CAS  Google Scholar 

  • Willenz P, Van de Vyver G (1982) 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. J Ultrastruct Res 79(3):294–306

    Article  PubMed  CAS  Google Scholar 

  • Wood RL (1979) The fine structure of the hypostome and mouth of Hydra. II. Transmission electron microscopy. Cell Tissue Res 199(2):319–338

    Article  PubMed  CAS  Google Scholar 

  • Wright KA (1991) Nematoda. In: Harrison FW, Ruppert EE (eds). Microscopic anatomy of invertebrates, vol. 4. Wiley: New York, pp 111–195

  • Xu N, Wang SQ, Tan D, Gao Y, Lin G, Xi R (2011) EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. Dev Biol 354(1):31–43

    Article  PubMed  CAS  Google Scholar 

  • Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY (2001) Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294:2155–2158

    Article  PubMed  CAS  Google Scholar 

  • Yasuo H, Lemaire P (1999) A two-step model for the fate determination of presumptive endodermal blastomeres in Xenopus embryos. Curr Biol 9(16):869–879

    Article  PubMed  CAS  Google Scholar 

  • Yen TH, Wright NA (2006) The gastrointestinal tract stem cell niche. Stem Cell Rev 2(3):203–212

    Article  PubMed  CAS  Google Scholar 

  • Yeung TM, Chia LA, Kosinski CM, Kuo CJ (2011) Regulation of self-renewal and differentiation by the intestinal stem cell niche. Cell Mol Life Sci 68(15):2513–2525

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Houston DW, King ML, Payne C, Wylie C, Heasman J (1998) The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell 94(4):515–524

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Hill RJ, Heid PJ, Fukuyama M, Sugimoto A, Priess JR, Rothman JH (1997) end-1 encodes an apparent GATA factor that specifies the endoderm precursor in Caenorhabditis elegans embryos. Genes Dev 11(21):2883–2896

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Grant NIH/1 R01 GM087373 to Volker Hartenstein. DAG gratefully acknowledges funding from an NIH Training Grant in Genomic Analysis and Interpretation T32HG002536 and the National Aeronautics and Space Administration (NASA) Astrobiology Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Volker Hartenstein.

Additional information

Communicated by: Ralf Sommer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takashima, S., Gold, D. & Hartenstein, V. Stem cells and lineages of the intestine: a developmental and evolutionary perspective. Dev Genes Evol 223, 85–102 (2013). https://doi.org/10.1007/s00427-012-0422-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-012-0422-8

Keywords

Navigation