PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan

Cell

Volumn 156, Issue 1-2, 2014, Pages 109-122

  Guo, Linlin ^a,b   Karpac, Jason ^a   Tran, Susan L ^c   Jasper, Heinrich ^a,c  

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

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PEPTIDOGLYCAN RECOGNITION PROTEIN; PEPTIDOGLYCAN RECOGNITION PROTEIN SC2; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR REL; TRANSCRIPTOME; UNCLASSIFIED DRUG; MIFEPRISTONE;

AGING; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; COMMENSALISM; CONTROLLED STUDY; DROSOPHILA; DYSBIOSIS; DYSPLASIA; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; INTESTINE; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE FLORA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; TRANSCRIPTION REGULATION; ADULT; ANIMAL TISSUE; COLONY FORMING UNIT; COMMENSAL; FEMALE; INTESTINE FUNCTION DISORDER; LIFE EXTENSION; LONGEVITY; MICROBIOME; MICROSCOPY; PATHOGEN LOAD; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSGENE;

ANIMALS; CARRIER PROTEINS; CYTOKINES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; DYSBIOSIS; FORKHEAD TRANSCRIPTION FACTORS; HOMEOSTASIS; IMMUNITY, INNATE; INTESTINES; LONGEVITY; MODELS, ANIMAL; TRANSCRIPTOME;

EID: 84892714390     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.12.018     Document Type: Article

References (74)

1. A. Amcheslavsky, J. Jiang, and Y.T. Ip Tissue damage-induced intestinal stem cell division in Drosophila Cell Stem Cell 4 2009 49 61
2. Y. Apidianakis, C. Pitsouli, N. Perrimon, and L. Rahme Synergy between bacterial infection and genetic predisposition in intestinal dysplasia Proc. Natl. Acad. Sci. USA 106 2009 20883 20888
3. M. Bakula The persistence of a microbial flora during postembryogenesis of Drosophila melanogaster J. Invertebr. Pathol. 14 1969 365 374
4. T. Becker, G. Loch, M. Beyer, I. Zinke, A.C. Aschenbrenner, P. Carrera, T. Inhester, J.L. Schultze, and M. Hoch FOXO-dependent regulation of innate immune homeostasis Nature 463 2010 369 373
5. E. Biagi, M. Candela, S. Turroni, P. Garagnani, C. Franceschi, and P. Brigidi Ageing and gut microbes: perspectives for health maintenance and longevity Pharmacol. Res. 69 2013 11 20
6. V. Bischoff, C. Vignal, B. Duvic, I.G. Boneca, J.A. Hoffmann, and J. Royet Downregulation of the Drosophila immune response by peptidoglycan- recognition proteins SC1 and SC2 PLoS Pathog. 2 2006 e14
7. B. Biteau, and H. Jasper EGF signaling regulates the proliferation of intestinal stem cells in Drosophila Development 138 2011 1045 1055
8. B. Biteau, C.E. Hochmuth, and H. Jasper JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut Cell Stem Cell 3 2008 442 455
9. B. Biteau, J. Karpac, S. Supoyo, M. Degennaro, R. Lehmann, and H. Jasper Lifespan extension by preserving proliferative homeostasis in Drosophila PLoS Genet. 6 2010 e1001159
10. B. Biteau, C.E. Hochmuth, and H. Jasper Maintaining tissue homeostasis: dynamic control of somatic stem cell activity Cell Stem Cell 9 2011 402 411
11. B. Biteau, J. Karpac, D. Hwangbo, and H. Jasper Regulation of Drosophila lifespan by JNK signaling Exp. Gerontol. 46 2011 349 354
12. F. Bonnay, E. Cohen-Berros, M. Hoffmann, S.Y. Kim, G.L. Boulianne, J.A. Hoffmann, N. Matt, and J.M. Reichhart big bang gene modulates gut immune tolerance in Drosophila Proc. Natl. Acad. Sci. USA 110 2013 2957 2962
13. M. Boutros, H. Agaisse, and N. Perrimon Sequential activation of signaling pathways during innate immune responses in Drosophila Dev. Cell 3 2002 711 722
14. T. Brummel, A. Ching, L. Seroude, A.F. Simon, and S. Benzer Drosophila lifespan enhancement by exogenous bacteria Proc. Natl. Acad. Sci. USA 101 2004 12974 12979
15. N. Buchon, N.A. Broderick, S. Chakrabarti, and B. Lemaitre Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila Genes Dev. 23 2009 2333 2344
16. N. Buchon, N.A. Broderick, M. Poidevin, S. Pradervand, and B. Lemaitre Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation Cell Host Microbe 5 2009 200 211
17. N. Buchon, N.A. Broderick, T. Kuraishi, and B. Lemaitre Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection BMC Biol. 8 2010 152
18. N. Buchon, N.A. Broderick, and B. Lemaitre Gut homeostasis in a microbial world: insights from Drosophila melanogaster Nat. Rev. Microbiol. 11 2013 615 626
19. S. Chakrabarti, P. Liehl, N. Buchon, and B. Lemaitre Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut Cell Host Microbe 12 2012 60 70
20. M.C. Chambers, and D.S. Schneider Pioneering immunology: insect style Curr. Opin. Immunol. 24 2012 10 14
21. M. Chatterjee, and Y.T. Ip Pathogenic stimulation of intestinal stem cell response in Drosophila J. Cell. Physiol. 220 2009 664 671
22. H.Y. Chung, M. Cesari, S. Anton, E. Marzetti, S. Giovannini, A.Y. Seo, C. Carter, B.P. Yu, and C. Leeuwenburgh Molecular inflammation: underpinnings of aging and age-related diseases Ageing Res. Rev. 8 2009 18 30
23. M.J. Claesson, S. Cusack, O. O'Sullivan, R. Greene-Diniz, H. de Weerd, E. Flannery, J.R. Marchesi, D. Falush, T. Dinan, and G. Fitzgerald et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly Proc. Natl. Acad. Sci. USA 108 Suppl 1 2011 4586 4591
24. M.J. Claesson, I.B. Jeffery, S. Conde, S.E. Power, E.M. O'Connor, S. Cusack, H.M. Harris, M. Coakley, B. Lakshminarayanan, and O. O'Sullivan et al. Gut microbiota composition correlates with diet and health in the elderly Nature 488 2012 178 184
25. J.C. Clemente, L.K. Ursell, L.W. Parfrey, and R. Knight The impact of the gut microbiota on human health: an integrative view Cell 148 2012 1258 1270
26. J.R. DiAngelo, M.L. Bland, S. Bambina, S. Cherry, and M.J. Birnbaum The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling Proc. Natl. Acad. Sci. USA 106 2009 20853 20858
27. M. Fukuyama, K. Rokutan, T. Sano, H. Miyake, M. Shimada, and S. Tashiro Overexpression of a novel superoxide-producing enzyme, NADPH oxidase 1, in adenoma and well differentiated adenocarcinoma of the human colon Cancer Lett. 221 2005 97 104
28. S.I. Grivennikov, F.R. Greten, and M. Karin Immunity, inflammation, and cancer Cell 140 2010 883 899
29. E.M. Ha, C.T. Oh, Y.S. Bae, and W.J. Lee A direct role for dual oxidase in Drosophila gut immunity Science 310 2005 847 850
30. E.M. Ha, K.A. Lee, S.H. Park, S.H. Kim, H.J. Nam, H.Y. Lee, D. Kang, and W.J. Lee Regulation of DUOX by the Galphaq-phospholipase Cbeta-Ca2+ pathway in Drosophila gut immunity Dev. Cell 16 2009 386 397
31. E.M. Ha, K.A. Lee, Y.Y. Seo, S.H. Kim, J.H. Lim, B.H. Oh, J. Kim, and W.J. Lee Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in drosophila gut Nat. Immunol. 10 2009 949 957
32. C.E. Hochmuth, B. Biteau, D. Bohmann, and H. Jasper Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila Cell Stem Cell 8 2011 188 199
33. J.A. Hoffmann The immune response of Drosophila Nature 426 2003 33 38
34. L.V. Hooper, D.R. Littman, and A.J. Macpherson Interactions between the microbiota and the immune system Science 336 2012 1268 1273
35. H. Jasper, V. Benes, C. Schwager, S. Sauer, S. Clauder-Münster, W. Ansorge, and D. Bohmann The genomic response of the Drosophila embryo to JNK signaling Dev. Cell 1 2001 579 586
36. H. Jiang, P.H. Patel, A. Kohlmaier, M.O. Grenley, D.G. McEwen, and B.A. Edgar Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut Cell 137 2009 1343 1355
37. H. Jiang, M.O. Grenley, M.J. Bravo, R.Z. Blumhagen, and B.A. Edgar EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila Cell Stem Cell 8 2011 84 95
38. H. Jonsson, P. Allen, and S.L. Peng Inflammatory arthritis requires Foxo3a to prevent Fas ligand-induced neutrophil apoptosis Nat. Med. 11 2005 666 671
39. S. Kapuria, J. Karpac, B. Biteau, D. Hwangbo, and H. Jasper Notch-mediated suppression of TSC2 expression regulates cell differentiation in the Drosophila intestinal stem cell lineage PLoS Genet. 8 2012 e1003045
40. J. Karpac, A. Younger, and H. Jasper Dynamic coordination of innate immune signaling and insulin signaling regulates systemic responses to localized DNA damage Dev. Cell 20 2011 841 854
41. J. Karpac, B. Biteau, and H. Jasper Misregulation of an adaptive metabolic response contributes to the age-related disruption of lipid homeostasis in Drosophila Cell Rep. 4 2013 1250 1261
42. A. Kaser, S. Zeissig, and R.S. Blumberg Inflammatory bowel disease Annu. Rev. Immunol. 28 2010 573 621
43. T. Kim, and Y.J. Kim Overview of innate immunity in Drosophila J. Biochem. Mol. Biol. 38 2005 121 127
44. K.A. Lee, S.H. Kim, E.K. Kim, E.M. Ha, H. You, B. Kim, M.J. Kim, Y.G. Kwon, J.H. Ryu, and W.J. Lee Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila Cell 153 2013 797 811
45. F. Leulier, and J. Royet Maintaining immune homeostasis in fly gut Nat. Immunol. 10 2009 936 938
46. S. Libert, Y. Chao, X. Chu, and S.D. Pletcher Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NFkappaB signaling Aging Cell 5 2006 533 543
47. F. Maillet, V. Bischoff, C. Vignal, J. Hoffmann, and J. Royet The Drosophila peptidoglycan recognition protein PGRP-LF blocks PGRP-LC and IMD/JNK pathway activation Cell Host Microbe 3 2008 293 303
48. D. Mathur, A. Bost, I. Driver, and B. Ohlstein A transient niche regulates the specification of Drosophila intestinal stem cells Science 327 2010 210 213
49. S.E. McGuire, Z. Mao, and R.L. Davis Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila Sci. STKE 2004 2004 pl6
50. C.J. McLeod, L. Wang, C. Wong, and D.L. Jones Stem cell dynamics in response to nutrient availability Curr. Biol. 20 2010 2100 2105
51. C.A. Micchelli, and N. Perrimon Evidence that stem cells reside in the adult Drosophila midgut epithelium Nature 439 2006 475 479
52. A. Moskalev, and M. Shaposhnikov Pharmacological inhibition of NF-κB prolongs lifespan of Drosophila melanogaster Aging (Albany, N.Y. Online) 3 2011 391 394
53. A. Nenci, C. Becker, A. Wullaert, R. Gareus, G. van Loo, S. Danese, M. Huth, A. Nikolaev, C. Neufert, and B. Madison et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation Nature 446 2007 557 561
54. J.K. Nicholson, E. Holmes, J. Kinross, R. Burcelin, G. Gibson, W. Jia, and S. Pettersson Host-gut microbiota metabolic interactions Science 336 2012 1262 1267
55. L.E. O'Brien, S.S. Soliman, X. Li, and D. Bilder Altered modes of stem cell division drive adaptive intestinal growth Cell 147 2011 603 614
56. B. Ohlstein, and A. Spradling The adult Drosophila posterior midgut is maintained by pluripotent stem cells Nature 439 2006 470 474
57. E. Ottaviani, N. Ventura, M. Mandrioli, M. Candela, A. Franchini, and C. Franceschi Gut microbiota as a candidate for lifespan extension: an ecological/evolutionary perspective targeted on living organisms as metaorganisms Biogerontology 12 2011 599 609
58. J.C. Paredes, D.P. Welchman, M. Poidevin, and B. Lemaitre Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection Immunity 35 2011 770 779
59. S.L. Peng Forkhead transcription factors in chronic inflammation Int. J. Biochem. Cell Biol. 42 2010 482 485
60. C. Ren, P. Webster, S.E. Finkel, and J. Tower Increased internal and external bacterial load during Drosophila aging without life-span trade-off Cell Metab. 6 2007 144 152
61. M. Rera, S. Bahadorani, J. Cho, C.L. Koehler, M. Ulgherait, J.H. Hur, W.S. Ansari, T. Lo Jr., D.L. Jones, and D.W. Walker Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog Cell Metab. 14 2011 623 634
62. M. Rera, R.I. Clark, and D.W. Walker Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila Proc. Natl. Acad. Sci. USA 109 2012 21528 21533
63. J.H. Ryu, E.M. Ha, C.T. Oh, J.H. Seol, P.T. Brey, I. Jin, D.G. Lee, J. Kim, D. Lee, and W.J. Lee An essential complementary role of NF-kappaB pathway to microbicidal oxidants in Drosophila gut immunity EMBO J. 25 2006 3693 3701
64. J.H. Ryu, S.H. Kim, H.Y. Lee, J.Y. Bai, Y.D. Nam, J.W. Bae, D.G. Lee, S.C. Shin, E.M. Ha, and W.J. Lee Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila Science 319 2008 777 782
65. S. Saha, J. Qi, S. Wang, M. Wang, X. Li, Y.G. Kim, G. Núñez, D. Gupta, and R. Dziarski PGLYRP-2 and Nod2 are both required for peptidoglycan-induced arthritis and local inflammation Cell Host Microbe 5 2009 137 150
66. S. Saha, X. Jing, S.Y. Park, S. Wang, X. Li, D. Gupta, and R. Dziarski Peptidoglycan recognition proteins protect mice from experimental colitis by promoting normal gut flora and preventing induction of interferon-gamma Cell Host Microbe 8 2010 147 162
67. S.C. Shin, S.H. Kim, H. You, B. Kim, A.C. Kim, K.A. Lee, J.H. Yoon, J.H. Ryu, and W.J. Lee Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling Science 334 2011 670 674
68. M.T. Sorbara, and D.J. Philpott Peptidoglycan: a critical activator of the mammalian immune system during infection and homeostasis Immunol. Rev. 243 2011 40 60
69. G. Storelli, A. Defaye, B. Erkosar, P. Hols, J. Royet, and F. Leulier Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing Cell Metab. 14 2011 403 414
70. A.K. Tanenhaus, J. Zhang, and J.C. Yin In vivo circadian oscillation of dCREB2 and NF-κB activity in the Drosophila nervous system PLoS ONE 7 2012 e45130
71. K. Tominaga, T. Kawahara, T. Sano, K. Toida, Y. Kuwano, H. Sasaki, T. Kawai, S. Teshima-Kondo, and K. Rokutan Evidence for cancer-associated expression of NADPH oxidase 1 (Nox1)-based oxidase system in the human stomach Free Radic. Biol. Med. 43 2007 1627 1638
72. M.C. Wang, D. Bohmann, and H. Jasper JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila Dev. Cell 5 2003 811 816
73. K. Weber, N. Johnson, D. Champlin, and A. Patty Many P-element insertions affect wing shape in Drosophila melanogaster Genetics 169 2005 1461 1475
74. P. Zhang, M. Judy, S.J. Lee, and C. Kenyon Direct and indirect gene regulation by a life-extending FOXO protein in C. elegans: roles for GATA factors and lipid gene regulators Cell Metab. 17 2013 85 100