Haemocytes control stem cell activity in the Drosophila intestine

Nature Cell Biology

Volumn 17, Issue 6, 2015, Pages 736-748

  Ayyaz, Arshad ^a   Li, Hongjie ^a,b   Jasper, Heinrich ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 1; DECAPENTAPLEGIC PROTEIN; JANUS KINASE; PARAQUAT; RECEPTOR PROTEIN; SAXOPHONE PROTEIN; SMAD ON X PROTEIN; SMAD PROTEIN; STAT PROTEIN; THICKVEIN PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR; CELL SURFACE RECEPTOR; DPP PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; EGFR PROTEIN, DROSOPHILA; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN SERINE THREONINE KINASE; RECEPTOR; RECEPTOR REGULATED SMAD PROTEIN; SAX PROTEIN, DROSOPHILA; SMOX PROTEIN, DROSOPHILA; TKV PROTEIN, DROSOPHILA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ADULT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CELL ACTIVATION; CELL ACTIVITY; CELL INTERACTION; CELL MIGRATION; CELL NUCLEUS; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HOMEOSTASIS; INFECTION RESISTANCE; INTESTINAL NEURONAL DYSPLASIA; INTESTINAL STEM CELL; INTESTINE EPITHELIUM; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; UPREGULATION; ACTIVE TRANSPORT; ANIMAL; BIOSYNTHESIS; CELL CULTURE; COLORECTAL TUMOR; CYTOLOGY; DROSOPHILA MELANOGASTER; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INTESTINE MUCOSA; LIFE EXPECTANCY; METABOLISM; PATHOLOGY; REGENERATION; SECRETION (PROCESS); STEM CELL; TIGHT JUNCTION; TRANSGENIC ANIMAL; TRANSPLANTATION;

ACTIVE TRANSPORT, CELL NUCLEUS; AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL PROLIFERATION; CELLS, CULTURED; COLORECTAL NEOPLASMS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENZYME ACTIVATION; HEMOCYTES; IMMUNE TOLERANCE; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; JANUS KINASES; LIFE EXPECTANCY; MACROPHAGES; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CELL SURFACE; RECEPTORS, INVERTEBRATE PEPTIDE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; REGENERATION; SMAD PROTEINS, RECEPTOR-REGULATED; STEM CELLS; TIGHT JUNCTIONS;

EID: 84930160218     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3174     Document Type: Article

References (69)

1. Ferrandon, D. The complementary facets of epithelial host defenses in the genetic model organism Drosophila melanogaster: from resistance to resilience. Curr. Opin. Immunol. 25, 59-70 (2013)
2. Lemaitre, B. & Miguel-Aliaga, I. The digestive tract of Drosophila melanogaster. Annu. Rev. Genet. 47, 377-404 (2013)
3. Ostaff, M. J., Stange, E. F. & Wehkamp, J. Antimicrobial peptides and gut microbiota in homeostasis and pathology. EMBO Mol. Med. 5, 1465-1483 (2013)
4. Kaiko, G. E. & Stappenbeck, T. S. Host-microbe interactions shaping the gastrointestinal environment. Trends Immunol. 35, 538-548 (2014)
5. Buchon, N., Broderick, N. A. & Lemaitre, B. Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat. Rev. Microbiol. 11, 615-626 (2013)
6. Ayyaz, A. & Jasper, H. Intestinal inflammation and stem cell homeostasis in aging. Front. Cell. Infect. Microbiol. 3, 98 (2013)
7. Micchelli, C. A. & Perrimon, N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439, 475-479 (2006)
8. Ohlstein, B. & Spradling, A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439, 470-474 (2006)
9. Biteau, B., Hochmuth, C. E. & Jasper, H. Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. Cell Stem Cell 9, 402-411 (2011)
10. Jiang, H. et al. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137, 1343-1355 (2009)
11. Biteau, B. & Jasper, H. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 138, 1045-1055 (2011)
12. Xu, N. et al. EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. Dev. Biol. 354, 31-43 (2011)
13. Buchon, N., Broderick, N. A., Kuraishi, T. & Lemaitre, B. Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biol. 8, 152 (2010)
14. Jiang, H., Grenley, M. O., Bravo, M. J., Blumhagen, R. Z. & Edgar, B. A. EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell 8, 84-95 (2011)
15. Buchon, N., Broderick, N. A., Chakrabarti, S. & Lemaitre, B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 23, 2333-2344 (2009)
16. Cronin, S. J. F. et al. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 325, 340-343 (2009)
17. Cordero, J. B. & Sansom, O. J. Wnt signalling and its role in stem cell-driven intestinal regeneration and hyperplasia. Acta Physiol. 204, 137-143 (2012)
18. Li, H., Qi, Y. & Jasper, H. Dpp signaling determines regional stem cell identity in the regenerating adult Drosophila gastrointestinal tract. Cell Rep. 4, 10-18 (2013)
19. Li, Z., Zhang, Y., Han, L., Shi, L. & Lin, X. Trachea-derived dpp controls adult midgut homeostasis in Drosophila. Dev. Cell 24, 133-143 (2013)
20. Guo, Z., Driver, I. & Ohlstein, B. Injury-induced BMP signaling negatively regulates Drosophila midgut homeostasis. J. Cell Biol. 201, 945-961 (2013)
21. Tian, A. & Jiang, J. Intestinal epithelium-derived BMP controls stem cell self-renewal in Drosophila adult midgut. eLife 3, e01857 (2014)
22. Zhou, J. et al. Dpp/Gbb signaling is required for normal intestinal regeneration during infection. Dev. Biol. 399, 189-203 (2014)
23. Skoczek, D. A. et al. Luminal microbes promote monocyte-stem cell interactions across a healthy colonic epithelium. J. Immunol. 193, 439-451 (2014)
24. Pull, S. L., Doherty, J. M., Mills, J. C., Gordon, J. I. & Stappenbeck, T. S. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc. Natl Acad. Sci. USA 102, 99-104 (2005)
25. Malvin, N. P., Seno, H. & Stappenbeck, T. S. Colonic epithelial response to injury requires Myd88 signaling in myeloid cells. Mucosal Immunol. 5, 194-206 (2012)
26. Lemaitre, B. & Hoffmann, J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697-743 (2007)
27. Babcock, D. T. et al. Circulating blood cells function as a surveillance system for damaged tissue in Drosophila larvae. Proc. Natl Acad. Sci. USA 105, 10017-10022 (2008)
28. Charroux, B. & Royet, J. Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the Drosophila immune response. Proc. Natl Acad. Sci. USA 106, 9797-9802 (2009)
29. Zaidman-Remy, A., Regan, J. C., Brandao, A. S. & Jacinto, A. The Drosophila larva as a tool to study gut-associated macrophages: PI3K regulates a discrete hemocyte population at the proventriculus. Dev. Comp. Immunol. 36, 638-647 (2012)
30. Tokusumi, T., Shoue, D. A., Tokusumi, Y., Stoller, J. R. & Schulz, R. A. New hemocytespecific enhancer-reporter transgenes for the analysis of hematopoiesis in Drosophila. Genesis 47, 771-774 (2009)
31. Kurucz, E. et al. Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr. Biol. 17, 649-654 (2007)
32. Amcheslavsky, A., Jiang, J. & Ip, Y. T. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 4, 49-61 (2009)
33. Makhijani, K., Alexander, B., Tanaka, T., Rulifson, E. & Bruckner, K. The peripheral nervous system supports blood cell homing and survival in the Drosophila larva. Development 138, 5379-5391 (2011)
34. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254 (2001)
35. Zettervall, C. J. et al. A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl Acad. Sci. USA 101, 14192-14197 (2004)
36. Clark, R. I., Woodcock, K. J., Geissmann, F., Trouillet, C. & Dionne, M. S. Multiple TGF- superfamily signals modulate the adult Drosophila immune response. Curr. Biol. 21, 1672-1677 (2011)
37. Teleman, A. A. & Cohen, S. M. Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103, 971-980 (2000)
38. Harrison, D. A. & Perrimon, N. Simple and efficient generation of marked clones in Drosophila. Curr. Biol. 3, 424-433 (1993)
39. Bardet, P. L. et al. A fluorescent reporter of caspase activity for live imaging. Proc. Natl Acad. Sci. USA 105, 13901-13905 (2008)
40. Hamaratoglu, F., de Lachapelle, A. M., Pyrowolakis, G., Bergmann, S. & Affolter, M. Dpp signaling activity requires Pentagone to scale with tissue size in the growing Drosophila wing imaginal disc. PLoS Biol. 9, e1001182 (2011)
41. Brummel, T. J. et al. Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78, 251-261 (1994)
42. Henderson, K. D. & Andrew, D. J. Identification of a novel Drosophila SMAD on the X chromosome. Biochem. Biophys. Res. Commun. 252, 195-201 (1998)
43. Spokony, R. & White, K. Spokony Insertions (Flybase, 2013)
44. Zhu, C. C. et al. Drosophila Activin-and the Activin-like product Dawdle function redundantly to regulate proliferation in the larval brain. Development 135, 513-521 (2008)
45. Kim, M. J. & O'Connor, M. B. Anterograde activin signaling regulates postsynaptic membrane potential and GluRIIA/B abundance at the Drosophila neuromuscular junction. PLoS ONE 9, e107443 (2014)
46. Bangi, E. & Wharton, K. Dual function of the Drosophila Alk1/Alk2 ortholog Saxophone shapes the Bmp activity gradient in the wing imaginal disc. Development 133, 3295-3303 (2006)
47. Haerry, T. E., Khalsa, O., O'Connor, M. B. & Wharton, K. A. Synergistic signaling by two BMP ligands through the SAX and TKV receptors controls wing growth and patterning in Drosophila. Development 125, 3977-3987 (1998)
48. Biteau, B. et al. Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genet. 6, e1001159 (2010)
49. Guo, L., Karpac, J., Tran, S. L. & Jasper, H. PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell 156, 109-122 (2014)
50. Rera, M., Clark, R. I. & Walker, D. W. Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proc. Natl Acad. Sci. USA 109, 21528-21533 (2012)
51. Godwin, J. W., Pinto, A. R. & Rosenthal, N. A. Macrophages are required for adult salamander limb regeneration. Proc. Natl Acad. Sci. USA 110, 9415-9420 (2013)
52. Assoian, R. K. et al. Expression and secretion of type transforming growth factor by activated human macrophages. Proc. Natl Acad. Sci. USA 84, 6020-6024 (1987)
53. Miyoshi, H., Ajima, R., Luo, C. T., Yamaguchi, T. P. & Stappenbeck, T. S. Wnt5a potentiates TGF- signaling to promote colonic crypt regeneration after tissue injury. Science 338, 108-113 (2012)
54. Wakefield, L. M. & Hill, C. S. Beyond TGF: roles of other TGF superfamily members in cancer. Nat. Rev. Cancer 13, 328-341 (2013)
55. Peterson, A. J. & O'Connor, M. B. Strategies for exploring TGF- signaling in Drosophila. Methods 68, 183-193 (2014)
56. Twombly, V. et al. Functional analysis of saxophone, the Drosophila gene encoding the BMP type I receptor ortholog of human ALK1/ACVRL1 and ACVR1/ALK2. Genetics 183, 563-579 (2009) 1SI-8SI
57. Bangi, E. & Wharton, K. Dpp and Gbb exhibit different effective ranges in the establishment of the BMP activity gradient critical for Drosophila wing patterning. Dev. Biol. 295, 178-193 (2006)
58. Haerry, T. E. The interaction between two TGF-type I receptors plays important roles in ligand binding, SMAD activation, and gradient formation. Mech. Dev. 127, 358-370 (2010)
59. Brummel, T. et al. The Drosophila activin receptor baboon signals through dSmad2 and controls cell proliferation but not patterning during larval development. Genes Dev. 13, 98-111 (1999)
60. Wang, X., Harris, R. E., Bayston, L. J. & Ashe, H. L. Type IV collagens regulate BMP signalling in Drosophila. Nature 455, 72-77 (2008)
61. Li, C. Y., Guo, Z. & Wang, Z. TGF receptor saxophone non-autonomously regulates germline proliferation in a Smox/dSmad2-dependent manner in Drosophila testis. Dev. Biol. 309, 70-77 (2007)
62. Isogaya, K. et al. A Smad3 and TTF-1/NKX2-1 complex regulates Smad4-independent gene expression. Cell Res. 24, 994-1008 (2014)
63. Shaw, A. C., Goldstein, D. R. & Montgomery, R. R. Age-dependent dysregulation of innate immunity. Nat. Rev. Immunol. 13, 875-887 (2013)
64. Wang, G. C. & Casolaro, V. Immunologic changes in frail older adults. Transl. Med. UniSa 9, 1-6 (2014)
65. Khor, B., Gardet, A. & Xavier, R. J. Genetics and pathogenesis of inflammatory bowel disease. Nature 474, 307-317 (2011)
66. Wang, L., Zeng, X., Ryoo, H. D. & Jasper, H. Integration of UPRER and oxidative stress signaling in the control of intestinal stem cell proliferation. PLoS Genet. 10, e1004568 (2014)
67. Osterwalder, T., Yoon, K. S., White, B. H. & Keshishian, H. A conditional tissuespecific transgene expression system using inducible GAL4. Proc. Natl Acad. Sci. USA 98, 12596-12601 (2001)
68. Ni, J. Q. et al. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat. Methods 8, 405-407 (2011)
69. McGuire, S. E., Mao, Z. & Davis, R. L. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci. STKE 2004, pl6 (2004).