The adult Drosophila gastric and stomach organs are maintained by a multipotent stem cell pool at the foregut/midgut junction in the cardia (proventriculus)

References

• Brittan M, Wright NA. Sell S. Stem cell origin of cell lineages, proliferative units, and cancer in the gastrointestinal tract. Stem Cells Handbook Totowa 2002; NJ Humana Press 329 - 343
   Google Scholar
• McDonald SA, Preston SL, Lovell MJ, Wright NA, Jankowski JA. Mechanisms of disease: from stem cells to colorectal cancer. Nat Clin Pract Gastroenterol Hepatol 2006; 3:267 - 274
   PubMedGoogle Scholar
• Wright NA. Epithelial stem cell repertoire in the gut: clues to the origin of cell lineages, proliferative units and cancer. Int J Exp Path 2000; 81:117 - 143
   PubMed Web of Science ®Google Scholar
• Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55:74 - 108
   PubMed Web of Science ®Google Scholar
• Barker N, van de Wetering M, Clevers H. The intestinal stem cell. Genes Dev 2008; 22:1856 - 1864
   PubMed Web of Science ®Google Scholar
• Radtke F, Clevers H. Self-renewal and cancer of the gut: two sides of a coin. Science 2005; 307:1904 - 1909
   PubMed Web of Science ®Google Scholar
• Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007; 449:1003 - 1007
   PubMed Web of Science ®Google Scholar
• Bjerknes M, Cheng H. Multipotential stem cells in adult mouse gastric epithelium. Am J Physiol: Gastrointest Liver Physiol 2002; 283:G767 - G777
   PubMed Web of Science ®Google Scholar
• Karam SM, Straiton T, Hassan WM, Leblond CP. Defining epithelial cell progenitors in the human oxyntic mucosa. Stem Cells 2003; 21:322 - 336
   PubMed Web of Science ®Google Scholar
• Hoffmann W. Regeneration of the gastric mucosa and its glands from stem cells. Curr Med Chem 2008; 15:3133 - 3144
   PubMed Web of Science ®Google Scholar
• Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es J H, et al. Lgr5+ve stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 2010; 6:25 - 36
   PubMed Web of Science ®Google Scholar
• van den Brink G R, Hardwick JC, Tytgat GNJ, Brink MA, ten Kate FJ, van Deventer SJH, Peppelenbosch MP. Sonic hedgehog regulates gastric gland morphogenesis in man and mouse. Gastroenterology 2001; 121:317 - 328
   PubMed Web of Science ®Google Scholar
• Kouznetsova I, Kalinski T, Meyer F, Hoffmann W. Self-renewal of the human gastric epithelium: new insights from expression profiling using laser microdissection. Mol BioSyst 2011; 7:1105 - 1112; http://dx.doi.org/10.1039/C0MB00233J
   PubMed Web of Science ®Google Scholar
• Fox DT, Spradling AC. The Drosophila hindgut lacks constitutively active adult stem cells but proliferates in response to tissue damage. Cell Stem Cell 2009; 5:290 - 297
   PubMed Web of Science ®Google Scholar
• Micchelli CA, Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 2006; 39:475 - 479
   Web of Science ®Google Scholar
• Ohlstein B, Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 2006; 439:470 - 474
   PubMed Web of Science ®Google Scholar
• Takashima S, Mkrtchyan M, Younossi-Hartenstein A, Merriam JR, Hartenstein V. The behaviour of Drosophila adult hindgut stem cells is controlled by Wnt and Hh signaling. Nature 2008; 454:651 - 655
   PubMed Web of Science ®Google Scholar
• Ohlstein B, Spradling A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential Notch signaling. Science 2007; 315:988 - 992
   PubMed Web of Science ®Google Scholar
• Biteau B, Hochmuth CE, Jasper H. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 2008; 3:442 - 455
   PubMed Web of Science ®Google Scholar
• Shaw RL, Kohlmaier A, Polesello C, Veelken C, Edgar BA, Tapon N. The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 2010; 137:4147 - 4158
   PubMed Web of Science ®Google Scholar
• Bardin AJ, Perdigoto CN, Southall TD, Brand AH, Schweisguth F. Transcriptional control of stem cell maintenance in the Drosophila intestine. Development 2010; 137:705 - 714
   PubMed Web of Science ®Google Scholar
• Liu W, Singh SR, Hou SX. JAK-STAT is restrained by Notch to control cell proliferation of the Drosophila intestinal stem cells. J Cell Biochem 2010; 109:992 - 999
   PubMed Web of Science ®Google Scholar
• Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 2009; 137:1343 - 1355
   PubMed Web of Science ®Google Scholar
• Amcheslavsky A, Jiang J, Ip YT. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 2009; 4:49 - 61
   PubMed Web of Science ®Google Scholar
• Lee WC, Beebe K, Sudmeier L, Micchelli CA. Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation. Development 2009; 136:2255 - 2264
   PubMed Web of Science ®Google Scholar
• Buchon N, Broderick NA, Chakrabarti S, Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev 2009; 23:2333 - 2344
   PubMed Web of Science ®Google Scholar
• Lin G, Xu N, Xi R. Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 2008; 455:1119 - 1123
   PubMed Web of Science ®Google Scholar
• Lin G, Xu N, Xi R. Paracrine unpaired signaling through the JAK/STAT pathway controls self-renewal and lineage differentiation of Drosophila intestinal stem cells. J Mol Cell Biol. 2010; 2:37 - 49
   PubMed Web of Science ®Google Scholar
• King DG. Cellular organization and peritrophic membrane formation in the cardia (proventriculus) of Drosophila melanogaster. J Morphol 1988; 196:253 - 282
   PubMed Web of Science ®Google Scholar
• King DG. The origin of an organ: Phylogenetic analysis of evolutionary innovation in the digestive tract of flies (Insecta: Diptera). Evolution 1991; 45:568 - 588
   PubMed Web of Science ®Google Scholar
• Skaer H. Bate M, Martinez A. The alimentary canal. The Development of Drosophila melanogaster 1993; New York Cold Spring Harbor Laboratory Press 941 - 1012
   Google Scholar
• Fuss B, Josten F, Feix M, Hoch M. Cell movements controlled by the Notch signalling cascade during fore-gut development in Drosophila. Development 2004; 131:1587 - 1595
   PubMed Web of Science ®Google Scholar
• Jung S, Evans CJ, Uemura C, Banerjee U. Cooperation of JAK/STAT and Notch signaling in the Drosophila foregut. Dev Biol 2004; 267:181 - 189
   PubMed Web of Science ®Google Scholar
• Pankratz MJ, Hoch M. Control of epithelial morphogenesis by cell signaling and integrin molecules in the Drosophila foregut. Development 1995; 121:1885 - 1898
   PubMed Web of Science ®Google Scholar
• Bach EA, Ekas LA, Ayala-Camargo A, Flaherty MS, Lee H, Perrimon N, et al. GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr Patterns 2007; 7:323 - 331
   PubMed Web of Science ®Google Scholar
• Singh SR, Liu W, Hou SX. The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 2007; 1:191 - 203
   PubMed Web of Science ®Google Scholar
• Siddall NA, McLaughlin EA, Marriner NL, Hime GR. The RNA-binding protein Musashi is required intrinsically to maintain stem cell identity. Proc Natl Acad Sci USA 2006; 103:8402 - 8407
   PubMed Web of Science ®Google Scholar
• Edgar BA, Orr-Weaver TL. Endoreplication cell cycles: more for less. Cell 2001; 105:297 - 306
   PubMed Web of Science ®Google Scholar
• Harrison DA, Perrimon N. A simple and efficient generation of marked clones in Drosophila. Curr Biol 1993; 3:424 - 433
   PubMed Web of Science ®Google Scholar
• Lee T, Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999; 22:451 - 461
   PubMed Web of Science ®Google Scholar
• Jung S, Evans CJ, Uemura C, Banerjee U. The Drosophila lymph gland as a developmental model of hematopoiesis. Development 2005; 132:2521 - 2533
   PubMed Web of Science ®Google Scholar
• Struhl G, Basler K. Organizing activity of wingless protein in Drosophila. Cell 1993; 72:527 - 540
   PubMed Web of Science ®Google Scholar
• McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003; 302:1765 - 1768
   PubMed Web of Science ®Google Scholar
• van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, et al. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 1997; 88:789 - 799
   PubMed Web of Science ®Google Scholar
• Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118:401 - 415
   PubMed Web of Science ®Google Scholar
• Methot N, Basler K. Hedgehog controls limb development by regulating the activities of distinct transcriptional activator and repressor forms of Cubitus interruptus. Cell 1999; 96:819 - 831
   PubMed Web of Science ®Google Scholar
• Wang G, Wang B, Jiang J. Protein kinase A antagonizes Hedgehog signaling by regulating both the activator and repressor forms of Cubitus interruptus. Genes Dev 1999; 13:2828 - 2837
   PubMed Web of Science ®Google Scholar
• Decotto E, Spradling AC. The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev Cell 2005; 9:501 - 510
   PubMed Web of Science ®Google Scholar
• Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 2001; 294:2542 - 2545
   PubMed Web of Science ®Google Scholar
• Tulina N, Matunis E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 2001; 294:2546 - 2549
   PubMed Web of Science ®Google Scholar
• Leatherman JL, Dinardo S. Germline self-renewal requires cyst stem cells and stat regulates niche adhesion in Drosophila testes. Nat Cell Biol 2010; 12:806 - 811
   PubMed Web of Science ®Google Scholar
• Arbouzova NI, Zeidler MP. JAK/STAT signaling in Drosophila: insights into conserved regulatory and cellular functions. Development 2006; 133:1605 - 1616
   Web of Science ®Google Scholar
• Hou XS, Melnick MB, Perrimon N. marelle acts downstream of the Drosophila hop/JAK kinase and encodes a protein similar to the mammalian STATs. Cell 1996; 84:411 - 419
   PubMed Web of Science ®Google Scholar
• Yan R, Small S, Desplan C, Dearolf CR, Darnell JJ. Identification of a Stat gene that functions in Drosophila development. Cell 1996; 84:421 - 430
   PubMed Web of Science ®Google Scholar
• Baksa K, Parke T, Dobens LL, Dearolf CR. The Drosophila STAT protein, Stat92E, regulates follicle cell differentiation during oogenesis. Dev Biol 2002; 243:166 - 175
   PubMed Web of Science ®Google Scholar
• Harrison DA, McCoon PE, Binari R, Gilman M, Perrimon N. Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev 1998; 12:3252 - 3263
   PubMed Web of Science ®Google Scholar
• Brown S, Hu N, Hombria JC. Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr Biol 11:1700 - 1705
   PubMed Web of Science ®Google Scholar
• Chen HW, Chen X, Oh S, Marinissen MJ, Gutkind JS, Hou XS. mom identifies a receptor for the Drosophila JAK/STAT signal transduction pathway and encodes a protein distantly related to the mammalian cytokine receptor family. Genes Dev 2002; 16:388 - 398
   PubMed Web of Science ®Google Scholar
• Binari R, Perrimon N. Stripe-specific regulation of pair-rule genes by hopscotch, a putative Jak family tyrosine kinase in Drosophila. Genes Dev 1994; 8:300 - 312
   PubMed Web of Science ®Google Scholar
• Brawley C, Matunis E. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 2004; 304:1331 - 1334
   PubMed Web of Science ®Google Scholar
• Qiao XT, Ziel JW, McKimpson W, Madison BB, Todisco A, Merchant JL, et al. Prospective identification of a multilineage progenitor in murine stomach epithelium. Gastroenterology 2007; 133:1989 - 1998
   PubMed Web of Science ®Google Scholar
• Gong W, Wang L, Yao JC, Ajani JA, Wei D, Aldape KD, et al. Expression of activated signal transducer and activator of transcription 3 predicts expression of vascular endothelial growth factor in and angiogenic phenotype of human gastric cancer. Clin Cancer Res 2005; 11:1386 - 1393
   PubMed Web of Science ®Google Scholar
• Oguma K, Oshima H, Aoki M, Uchio R, Naka K, Nakamura S, et al. Activated macrophages promote Wnt signalling through tumour necrosis factor-alpha in gastric tumour cells. EMBO J 2008; 27:1671 - 1681
   PubMed Web of Science ®Google Scholar
• Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 1998; 19:379 - 383
   PubMed Web of Science ®Google Scholar
• Nguyen H, Merrill BJ, Polak L, Nikolova M, Rendl M, Shaver TM, et al. Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nat Genet 2009; 41:1068 - 1075
   PubMed Web of Science ®Google Scholar
• Morrison SJ, Spradling AC. Stem cell and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008; 132:598 - 611
   PubMed Web of Science ®Google Scholar
• Wang H, Singh SR, Zheng Z, Oh SW, Chen X, Edwards K, Hou SX. A Rap-GEF/Rap GTPase signaling controls stem cell maintenance through regulating adherens junction positioning and cell adhesion in Drosophila testis. Dev Cell 2006; 10:117 - 126
   PubMed Web of Science ®Google Scholar
• Zeidler MP, Perrimon N, Strutt DI. The four-jointed gene is required in the Drosophila eye for ommatidial polarity specification. Curr Biol 1999; 9:1363 - 1372
   PubMed Web of Science ®Google Scholar
• Singh SR, Zhen W, Zheng Z, Wang H, Oh SW, Liu W, et al. The Drosophila homologue of the human tumor suppressor gene BHD regulates male germline stem cell maintenance and functions downstream of Dpp. Oncogene 2006; 25:5933 - 5941
   PubMed Web of Science ®Google Scholar
• Zeng X, Singh SR, Hou D, Hou SX. Tumor suppressors Sav/Scrib and oncogene Ras regulate stem-cell transformation in adult Drosophila malpighian tubules. J Cell Physiol 2010; 224:766 - 774
   PubMed Web of Science ®Google Scholar
• Singh SR, Zheng Z, Wang H, Oh SW, Chen X, Hou SX. Competitiveness for the niche and mutual dependence of the germline and somatic stem cells in the Drosophila testis are regulated by the JAK/STAT signaling. J Cell Physiol 2010; 223:500 - 510
   PubMed Web of Science ®Google Scholar
• Zeng X, Chauhan C, Hou SX. Characterization of midgut stem cell- and enteroblast-specific Gal4 lines in Drosophila. Genesis 2010; 48:607 - 611
   PubMed Web of Science ®Google Scholar