Intestinal epithelium-derived BMP controls stem cell self-renewal in Drosophila adult midgut

eLife

Volumn 2014, Issue 3, 2014, Pages

  Tian, Aiguo ^a   Jiang, Jin ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GELATINASE A; NOTCH RECEPTOR; COLLAGEN TYPE 4; DPP PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; GBB PROTEIN, DROSOPHILA; NOTCH PROTEIN, DROSOPHILA; TRANSFORMING GROWTH FACTOR BETA;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; DROSOPHILA; FEEDING; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE OVEREXPRESSION; GENOTYPE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INTESTINE CELL; INTESTINE EPITHELIUM; MIDGUT; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA HYBRIDIZATION; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL NICHE; TISSUE REGENERATION; TRANSGENE; WESTERN BLOTTING; ADULT STEM CELL; ANIMAL; CELL COMMUNICATION; CELL PROLIFERATION; CYTOLOGY; DROSOPHILA MELANOGASTER; GENETICS; INTESTINE; METABOLISM; MUTATION; PHENOTYPE; RNA INTERFERENCE; TRANSGENIC ANIMAL;

ADULT STEM CELLS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL COMMUNICATION; CELL PROLIFERATION; COLLAGEN TYPE IV; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENTEROCYTES; GENOTYPE; INTESTINES; MUTATION; PHENOTYPE; RECEPTORS, NOTCH; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEM CELL NICHE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84898762338     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01857     Document Type: Article

References (65)

1. Amcheslavsky A, Ito N, Jiang J, Ip YT. 2011. Tuberous sclerosis complex and Myc coordinate the growth and division of Drosophila intestinal stem cells. The Journal of Cell Biology 193:695-710. doi: 10.1083/jcb.201103018.
2. Amcheslavsky A, Jiang J, Ip YT. 2009. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 4:49-61. doi: 10.1016/j.stem.2008.10.016.
3. Auclair BA, Benoit YD, Rivard N, Mishina Y, Perreault N. 2007. Bone morphogenetic protein signaling is essential for terminal differentiation of the intestinal secretory cell lineage. Gastroenterology 133:887-896. doi: 10.1053/j.gastro.2007.06.066.
4. Axelrod JD. 2010. Delivering the lateral inhibition punchline: it's all about the timing. Science Signaling 3:pe38. doi: 10.1126/scisignal.3145pe38.
5. Ballard SL, Jarolimova J, Wharton KA. 2010. Gbb/BMP signaling is required to maintain energy homeostasis in Drosophila. Developmental Biology 337:375-385. doi: 10.1016/j.ydbio.2009.11.011.
6. Bardin AJ, Perdigoto CN, Southall TD, Brand AH, Schweisguth F. 2010. Transcriptional control of stem cell maintenance in the Drosophila intestine. Development 137:705-714. doi: 10.1242/dev.039404.
7. Biteau B, Hochmuth CE, Jasper H. 2008. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3:442-455. doi: 10.1016/j.stem.2008.07.024.
8. Biteau B, Hochmuth CE, Jasper H. 2011. Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. Cell Stem Cell 9:402-411. doi: 10.1016/j.stem.2011.10.004.
9. Biteau B, Jasper H. 2011. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 138:1045-1055. doi: 10.1242/dev.056671.
10. Brummel TJ, Twombly V, Marques G, Wrana JL, Newfeld SJ, Attisano L, Massague J, O'Connor MB, Gelbart WM. 1994. Characterization and relationship of Dpp receptors encoded by saxophone and thick veins genes in Drosophila. Cell 78:251-261.
11. Buchon N, Broderick NA, Chakrabarti S, Lemaitre B. 2009. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes & Develpoment 23:2333-2344. doi: 10.1101/gad.1827009.
12. Buchon N, Osman D, David FP, Fang HY, Boquete JP, Deplancke B, Lemaitre B. 2013. Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Reports 3:1725-1738. doi: 10.1016/j.celrep.2013.04.001.
13. Casali A, Batlle E. 2009. Intestinal stem cells in mammals and Drosophila. Cell Stem Cell 4:124-127. doi: 10.1016/j.stem.2009.01.009.
14. Cooper MT, Bray SJ. 1999. Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 397:526-530. doi: 10.1038/17395.
15. Cordero JB, Stefanatos RK, Scopelliti A, Vidal M, Sansom OJ. 2012. Inducible progenitor-derived Wingless regulates adult midgut regeneration in Drosophila. The EMBO Journal 31:3901-3917. doi: 10.1038/emboj.2012.248.
16. de Navascues J, Perdigoto CN, Bian Y, Schneider MH, Bardin AJ, Martinez-Arias A, Simons BD. 2012. Drosophila midgut homeostasis involves neutral competition between symmetrically dividing intestinal stem cells. The EMBO Journal 31:2473-2485. doi: 10.1038/emboj.2012.106.
17. Entchev EV, Schwabedissen A, Gonzalez-Gaitan M. 2000. Gradient formation of the TGF-beta homolog Dpp. Cell 103:981-991. doi: 10.1016/S0092-8674(00)00200-2.
18. Fanto M, Mlodzik M. 1999. Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397:523-526. doi: 10.1038/17389.
19. Goulas S, Conder R, Knoblich JA. 2012. The par complex and integrins direct asymmetric cell division in adult intestinal stem cells. Cell Stem Cell 11:529-540. doi: 10.1016/j.stem.2012.06.017.
20. Guo Z, Driver I, Ohlstein B. 2013. Injury-induced BMP signaling negatively regulates Drosophila midgut homeostasis. Journal of Cell Biology 201:945-961. doi: 10.1083/jcb.201302049.
21. Haramis AP, Begthel H, van den Born M, van Es J, Jonkheer S, Offerhaus GJ, Clevers H. 2004. De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 303:1684-1686. doi: 10.1126/science.1093587.
22. He XC, Zhang J, Tong WG, Tawfik O, Ross J, Scoville DH, Tian Q, Zeng X, He X, Wiedemann LM, Mishina Y, Li L. 2004. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nature Genetics 36:1117-1121. doi: 10.1038/ng1430.
23. Jiang H, Edgar BA. 2012. Intestinal stem cell function in Drosophila and mice. Current Opinion in Genetics & Development 22:354-360. doi: 10.1016/j.gde.2012.04.002.
24. 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 8:84-95. doi: 10.1016/j.stem.2010.11.026.
25. 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 137:1343-1355. doi: 10.1016/j.cell.2009.05.014.
26. Jones DL, Wagers AJ. 2008. No place like home: anatomy and function of the stem cell niche. Nature Reviews Molecular Cell Biology 9:11-21. doi: 10.1038/nrm2319.
27. Karpowicz P, Perez J, Perrimon N. 2010. The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137:4135-4145. doi: 10.1242/dev.060483.
28. Khalsa O, Yoon JW, Torres-Schumann S, Wharton KA. 1998. TGF-beta/BMP superfamily members, Gbb-60A and Dpp, cooperate to provide pattern information and establish cell identity in the Drosophila wing. Development 125:2723-2734.
29. Kim BG, Li C, Qiao W, Mamura M, Kasprzak B, Anver M, Wolfraim L, Hong S, Mushinski E, Potter M, Kim SJ, Fu XY, Deng C, Letterio JJ. 2006. Smad4 signalling in T cells is required for suppression of gastrointestinal cancer. Nature 441:1015-1019. doi: 10.1038/nature04846.
30. Lee T, Luo L. 2001. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends in Neurosciences 24:251-254. doi: 10.1016/S0166-2236(00)01791-4.
31. Lee WC, Beebe K, Sudmeier L, Micchelli CA. 2009. Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation. Development 136:2255-2264. doi: 10.1242/dev.035196.
32. Li H, Qi Y, Jasper H. 2013a. Dpp signaling determines regional stem cell identity in the regenerating adult Drosophila gastrointestinal tract. Cell Reports 4:10-18. doi: 10.1016/j.celrep.2013.05.040.
33. Li Z, Zhang Y, Han L, Shi L, Lin X. 2013b. Trachea-derived dpp controls adult midgut homeostasis in Drosophila. Developmental Cell 24:133-143. doi: 10.1016/j.devcel.2012.12.010.
34. Lin G, Xu N, Xi R. 2008. Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 455:1119-1123. doi: 10.1038/nature07329.
35. Losick VP, Morris LX, Fox DT, Spradling A. 2011. Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Developmental Cell 21:159-171. doi: 10.1016/j.devcel.2011.06.018.
36. Marianes A, Spradling AC. 2013. Physiological and stem cell compartmentalization within the Drosophila midgut. ELife 2:e00886. doi: 10.7554/eLife.00886.
37. McGuire SE, Mao Z, Davis RL. 2004. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Science's STKE 2004:pl6. doi: 10.1126/stke.2202004pl6.
38. McLeod CJ, Wang L, Wong C, Jones DL. 2010. Stem cell dynamics in response to nutrient availability. Current Biology: CB 20:2100-2105. doi: 10.1016/j.cub.2010.10.038.
39. Micchelli CA, Perrimon N. 2006. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439:475-479. doi: 10.1038/nature04371.
40. Morrison SJ, Spradling AC. 2008. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132:598-611. doi: 10.1016/j.cell.2008.01.038.
41. Moustakas A, Heldin CH. 2009. The regulation of TGFbeta signal transduction. Development 136:3699-3714. doi: 10.1242/dev.030338.
42. Nahm M, Long AA, Paik SK, Kim S, Bae YC, Broadie K, Lee S. 2010. The Cdc42-selective GAP rich regulates postsynaptic development and retrograde BMP transsynaptic signaling. Journal of Cell Biology 191:661-675. doi: 10.1083/jcb.201007086.
43. Nellen D, Affolter M, Basler K. 1994. Receptor serine/Threonine kinase implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78:225-237. doi: 10.1016/0092-8674(94)90293-3.
44. Nellen D, Burke R, Struhl G, Basler K. 1996. Direct and long-range Action of a dpp Morphogen gradient. Cell 85:357-368. doi: 10.1016/j.mod.2008.12.002.
45. O'Brien LE, Soliman SS, Li X, Bilder D. 2011. Altered modes of stem cell division drive adaptive intestinal growth. Cell 147:603-614. doi: 10.1016/j.cell.2011.08.048.
46. Oh H, Irvine KD. 2011. Cooperative regulation of growth by Yorkie and Mad through bantam. Developmental Cell 20:109-122. doi: 10.1016/j.devcel.2010.12.002.
47. Ohlstein B, Spradling A. 2006. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470-474. doi: 10.1038/nature04333.
48. Ohlstein B, Spradling A. 2007. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 315:988-992. doi: 10.1126/science.1136606.
49. Oshimori N, Fuchs E. 2012. The harmonies played by TGF-beta in stem cell biology. Cell Stem Cell 11:751-764. doi: 10.1016/j.stem.2012.11.001.
50. Persson U, Izumi H, Souchelnytskyi S, Itoh S, Grimsby S, Engstrom U, Heldin CH, Funa K, ten Dijke P. 1998. The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. FEBS Letters 434:83-87. doi: 10.1016/S0014-5793(98)00954-5.
51. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S. 2008. Imaging individual mRNA molecules using multiple singly labeled probes. Nature Methods 5:877-879. doi: 10.1038/nmeth.1253.
52. Ray RP, Wharton KA. 2001. Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disk. Development 128:3913-3925.
53. Ren F, Shi Q, Chen Y, Jiang A, Ip YT, Jiang H, Jiang J. 2013. Drosophila Myc integrates multiple signaling pathways to regulate intestinal stem cell proliferation during midgut regeneration. Cell Research 23:1133-1146. doi: 10.1038/cr.2013.101.
54. Ren F, Wang B, Yue T, Yun EY, Ip YT, Jiang J. 2010. Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proceedings of the National Academy of Sciences of the United States of America 107:21064-21069. doi: 10.1073/pnas.1012759107.
55. Roy S, Hsiung F, Kornberg TB. 2011. Specificity of Drosophila cytonemes for distinct signaling pathways. Science 332:354-358. doi: 10.1126/science.1198949.
56. Ruberte E, Marty T, Nellen D, Affolter M, Basler K. 1995. An absolute requirement for both type II and type I receptors, punt and thick veins, for dpp signaling in vivo. Cell 80:889-897. doi: 10.1016/0092-8674(95)90292-9.
57. 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 137:4147-4158. doi: 10.1242/dev.052506.
58. Shimmi O, Umulis D, Othmer H, O'Connor MB. 2005. Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120:873-886. doi: 10.1016/j.cell.2005.02.009.
59. Staley BK, Irvine KD. 2010. Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Current Biology 20:1580-1587. doi: 10.1016/j.cub.2010.07.041.
60. Struhl G, Fitzgerald K, Greenwald I. 1993. Intrinsic activity of the lin-12 and Notch intracellular domains in vivo. Cell 74:331-345. doi: 10.1016/0092-8674(93)90424-O.
61. Teleman AA, Cohen SM. 2000. Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103:971-980. doi: 10.1016/S0092-8674(00)00199-9.
62. Wang X, Harris RE, Bayston LJ, Ashe HL. 2008. Type IV collagens regulate BMP signalling in Drosophila. Nature 455:72-77. doi: 10.1038/nature07214.
63. 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. Developmental Biology 354:31-43. doi: 10.1016/j.ydbio.2011.03.018.
64. Zeng X, Chauhan C, Hou SX. 2010. Characterization of midgut stem cell-and enteroblast-specific Gal4 lines in drosophila. Genesis 48:607-611. doi: 10.1002/dvg.20661.
65. Zhang J, Li L. 2005. BMP signaling and stem cell regulation. Developmental Biology 284:1-11. doi: 10.1016/j.ydbio.2005.05.009.