PERK Limits Drosophila Lifespan by Promoting Intestinal Stem Cell Proliferation in Response to ER Stress

PLoS Genetics

Volumn 11, Issue 5, 2015, Pages

  Wang, Lifen ^a   Ryoo, Hyung Don ^b   Qi, Yanyan ^a   Jasper, Heinrich ^a  

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

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE; PKR LIKE ENDOPLASMIC RETICULUM KINASE; PROTEIN KINASE; STAT PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; ERO1L PROTEIN, DROSOPHILA; OXIDOREDUCTASE; PERK KINASE; PROTEIN KINASE R; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA; DYSPLASIA; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FEMALE; INTESTINAL STEM CELL; LIFE EXTENSION; MALE; NONHUMAN; OXIDATION REDUCTION STATE; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; CYTOLOGY; GENETICS; HOMEOSTASIS; INTESTINE; METABOLISM; OXIDATIVE STRESS; PHOSPHORYLATION; SEQUENCE ANALYSIS; STEM CELL;

ANIMALS; CELL PROLIFERATION; DROSOPHILA; DROSOPHILA PROTEINS; EIF-2 KINASE; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; INTESTINES; OXIDATIVE STRESS; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; STEM CELLS; UNFOLDED PROTEIN RESPONSE;

EID: 84930787599     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005220     Document Type: Article

References (63)

1. Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, et al. (2008) Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS medicine 5: e54. doi: 10.1371/journal.pmed.0050054 18318598
2. Zhao F, Edwards R, Dizon D, Afrasiabi K, Mastroianni JR, et al. (2010) Disruption of Paneth and goblet cell homeostasis and increased endoplasmic reticulum stress in Agr2-/- mice. Developmental Biology 338: 270–279. doi: 10.1016/j.ydbio.2009.12.008 20025862
3. Messlik A, Schmechel S, Kisling S, Bereswill S, Heimesaat MM, et al. (2009) Loss of Toll-like receptor 2 and 4 leads to differential induction of endoplasmic reticulum stress and proapoptotic responses in the intestinal epithelium under conditions of chronic inflammation. Journal of proteome research 8: 4406–4417. doi: 10.1021/pr9000465 19681597
4. Kaser A, Lee A-H, Franke A, Glickman JN, Zeissig S, et al. (2008) XBP1 Links ER Stress to Intestinal Inflammation and Confers Genetic Risk for Human Inflammatory Bowel Disease. Cell 134: 743–756. doi: 10.1016/j.cell.2008.07.021 18775308
5. Niederreiter L, Fritz TMJ, Adolph TE, Krismer AM, Offner FA, et al. (2013) ER stress transcription factor Xbp1 suppresses intestinal tumorigenesis and directs intestinal stem cells. Journal of Experimental Medicine 210: 2041–2056. doi: 10.1084/jem.20122341 24043762
6. Glimcher LH, (2009) XBP1: the last two decades. Annals of the Rheumatic Diseases 69: i67–i71.
7. Garrett WS, Gordon JI, Glimcher LH, (2010) Homeostasis and inflammation in the intestine. Cell 140: 859–870. doi: 10.1016/j.cell.2010.01.023 20303876
8. Kaser A, Zeissig S, Blumberg RS, (2010) Inflammatory bowel disease. Annu Rev Immunol 28: 573–621. doi: 10.1146/annurev-immunol-030409-101225 20192811
9. Kaser A, Flak MB, Tomczak MF, Blumberg RS, (2011) The unfolded protein response and its role in intestinal homeostasis and inflammation. Experimental Cell Research 317: 2772–2779. doi: 10.1016/j.yexcr.2011.07.008 21821022
10. Adolph TE, Tomczak MF, Niederreiter L, Ko H-J, Böck J, et al. (2013) Paneth cells as a site of origin for intestinal inflammation. Nature 503: 272–276. doi: 10.1038/nature12599 24089213
11. Heijmans J, van Lidth de Jeude JF, Koo B-K, Rosekrans SL, Wielenga MCB, et al. (2013) ER Stress Causes Rapid Loss of Intestinal Epithelial Stemness through Activation of the Unfolded Protein Response. Cell reports 3: 1128–1139. doi: 10.1016/j.celrep.2013.02.031 23545496
12. Wang L, Zeng X, Ryoo HD, Jasper H, (2014) Integration of UPRER and Oxidative Stress Signaling in the Control of Intestinal Stem Cell Proliferation. PLoS Genet 10: e1004568. doi: 10.1371/journal.pgen.1004568 25166757
13. Walter P, Ron D, (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334: 1081–1086. doi: 10.1126/science.1209038 22116877
14. Shi Y, Vattem KM, Sood R, An J, Liang J, et al. (1998) Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 18: 7499–7509. 9819435
15. Harding HP, Zhang Y, Ron D, (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271–274. 9930704
16. Schröder M, Kaufman RJ, (2005) THE MAMMALIAN UNFOLDED PROTEIN RESPONSE. Annu Rev Biochem 74: 739–789. 15952902
17. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, et al. (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249–258. 10847680
18. Ryoo HD, Steller H, (2007) Unfolded protein response in Drosophila: why another model can make it fly. Cell Cycle 6: 830–835. 17387279
19. Smith MH, Ploegh HL, Weissman JS, (2011) Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334: 1086–1090. doi: 10.1126/science.1209235 22116878
20. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, et al. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11: 619–633. 12667446
21. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D, (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5: 897–904. 10882126
22. Han J, Back SH, Hur J, Lin Y-H, Gildersleeve R, et al. (2013) ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 15: 481–490. doi: 10.1038/ncb2738 23624402
23. Cullinan SB, Diehl JA, (2006) Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. The international journal of biochemistry & cell biology 38: 317–332.
24. Glover-Cutter KM, Lin S, Blackwell TK, (2013) Integration of the Unfolded Protein and Oxidative Stress Responses through SKN-1/Nrf. PLoS Genet 9: e1003701. doi: 10.1371/journal.pgen.1003701 24068940
25. Henis-Korenblit S, Zhang P, Hansen M, McCormick M, Lee SJ, et al. (2010) Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proceedings of the National Academy of Sciences 107: 9730–9735. doi: 10.1073/pnas.1002575107 20460307
26. Kourtis N, Tavernarakis N, (2011) Cellular stress response pathways and ageing: intricate molecular relationships. EMBO J 30: 2520–2531. doi: 10.1038/emboj.2011.162 21587205
27. Taylor RC, Dillin A, (2011) Aging as an event of proteostasis collapse. Cold Spring Harbor perspectives in biology 3.
28. Taylor RC, Dillin A, (2013) XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153: 1435–1447. doi: 10.1016/j.cell.2013.05.042 23791175
29. Frand AR, Kaiser CA, (1999) Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol Cell 4: 469–477. 10549279
30. Kim S, Sideris DP, Sevier CS, Kaiser CA, (2012) Balanced Ero1 activation and inactivation establishes ER redox homeostasis. The Journal of Cell Biology 196: 713–725. doi: 10.1083/jcb.201110090 22412017
31. Gross E, Sevier CS, Heldman N, Vitu E, Bentzur M, et al. (2006) Generating disulfides enzymatically: reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc Natl Acad Sci USA 103: 299–304. 16407158
32. Owusu-Ansah E, Banerjee U, (2009) Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461: 537–541. doi: 10.1038/nature08313 19727075
33. Noble M, Smith J, Power J, Mayer-Proschel M, (2003) Redox state as a central modulator of precursor cell function. Annals of the New York Academy of Sciences 991: 251–271. 12846992
34. Hochmuth CE, Biteau B, Bohmann D, Jasper H, (2011) Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell 8: 188–199. doi: 10.1016/j.stem.2010.12.006 21295275
35. Tothova Z, Gilliland DG, (2007) FoxO transcription factors and stem cell homeostasis: insights from the hematopoietic system. Cell Stem Cell 1: 140–152. doi: 10.1016/j.stem.2007.07.017 18371346
36. Micchelli CA, Perrimon N, (2006) Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439: 475–479. 16340959
37. Ohlstein B, Spradling A, (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439: 470–474. 16340960
38. 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 22056138
39. Biteau B, Jasper H, (2014) Slit/Robo signaling regulates cell fate decisions in the intestinal stem cell lineage of Drosophila. Cell reports 7: 1867–1875. doi: 10.1016/j.celrep.2014.05.024 24931602
40. Buchon N, Broderick NA, Lemaitre B, (2013) Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nature reviews Microbiology 11: 615–626. doi: 10.1038/nrmicro3074 23893105
41. 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 18940735
42. Choi NH, Kim JG, Yang DJ, Kim YS, Yoo MA, (2008) Age-related changes in Drosophila midgut are associated with PVF2, a PDGF/VEGF-like growth factor. Aging Cell 7: 318–334. doi: 10.1111/j.1474-9726.2008.00380.x 18284659
43. Rera M, Clark RI, Walker DW, (2012) Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proceedings of the National Academy of Sciences 109: 21528–21533. doi: 10.1073/pnas.1215849110 23236133
44. Biteau B, Karpac J, Supoyo S, DeGennaro M, Lehmann R, et al. (2010) Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genet 6: e1001159.
45. Guo L, Karpac J, Tran SL, Jasper H, (2014) PGRP-SC2 Promotes Gut Immune Homeostasis to Limit Commensal Dysbiosis and Extend Lifespan. Cell 156: 109–122. doi: 10.1016/j.cell.2013.12.018 24439372
46. Jasper H, Bohmann D, Jakob U, (2013) Redox Regulation of Stem Cell Function. In: Oxidative Stress and Redox Regulation. Springer Science & Business Media. 1 pp.
47. Sevier CS, Kaiser CA, (2008) Ero1 and redox homeostasis in the endoplasmic reticulum. Biochimica et biophysica acta 1783: 549–556. doi: 10.1016/j.bbamcr.2007.12.011 18191641
48. Tien AC, Rajan A, Schulze KL, Ryoo HD, Acar M, et al. (2008) Ero1L, a thiol oxidase, is required for Notch signaling through cysteine bridge formation of the Lin12-Notch repeats in Drosophila melanogaster. The Journal of Cell Biology 182: 1113–1125. doi: 10.1083/jcb.200805001 18809725
49. Roti G, Carlton A, Ross KN, Markstein M, Pajcini K, et al. (2013) Complementary genomic screens identify SERCA as a therapeutic target in NOTCH1 mutated cancer. Cancer cell 23: 390–405. doi: 10.1016/j.ccr.2013.01.015 23434461
50. Ryoo HD, Domingos PM, Kang M-J, Steller H, (2006) Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J 26: 242–252. 17170705
51. Sone M, Zeng X, Larese J, Ryoo HD, (2013) A modified UPR stress sensing system reveals a novel tissue distribution of IRE1/XBP1 activity during normal Drosophila development. Cell Stress Chaperones 18: 307–319. doi: 10.1007/s12192-012-0383-x 23160805
52. Dutta D, Xiang J, Edgar BA, (2013) RNA expression profiling from FACS-isolated cells of the Drosophila intestine. Current protocols in stem cell biology 27: Unit2F.2. doi: 10.1002/9780470151808.sc05a06s27 24510288
53. Zhou F, Rasmussen A, Lee S, Agaisse H, (2013) The UPD3 cytokine couples environmental challenge and intestinal stem cell division through modulation of JAK/STAT signaling in the stem cell microenvironment. Developmental Biology 373: 383–393. doi: 10.1016/j.ydbio.2012.10.023 23110761
54. Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, et al. (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 19563763
55. Bach EA, Ekas LA, Ayala-Camargo A, Flaherty MS, Lee H, et al. (2007) GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expression Patterns 7: 323–331. 17008134
56. Mathur D, Bost A, Driver I, Ohlstein B, (2010) A transient niche regulates the specification of Drosophila intestinal stem cells. Science 327: 210–213. doi: 10.1126/science.1181958 20056890
57. Petkau K, Parsons BD, Duggal A, Foley E, (2014) A deregulated intestinal cell cycle program disrupts tissue homeostasis without affecting longevity in Drosophila. Journal of Biological Chemistry 289: 28719–28729. doi: 10.1074/jbc.M114.578708 25170078
58. Rera M, Bahadorani S, Cho J, Koehler CL, Ulgherait M, et al. (2011) Modulation of Longevity and Tissue Homeostasis by the Drosophila PGC-1 Homolog. Cell Metab 14: 623–634. doi: 10.1016/j.cmet.2011.09.013 22055505
59. Kaser A, Blumberg RS, (n.d.) Endoplasmic reticulum stress and intestinal inflammation. Mucosal Immunol 3: 11–16. doi: 10.1038/mi.2009.122 19865077
60. Parker A, Watson AJM, (2014) Details unfold: the endoplasmic reticulum stress response in intestinal inflammation and cancer. Gastroenterology 147: 531–533. doi: 10.1053/j.gastro.2014.06.013 24953624
61. Berger E, Haller D, (2011) Structure-function analysis of the tertiary bile acid TUDCA for the resolution of endoplasmic reticulum stress in intestinal epithelial cells. Biochemical and biophysical research communications 409: 610–615. doi: 10.1016/j.bbrc.2011.05.043 21605547
62. Iannitti T, Palmieri B, (2011) Clinical and experimental applications of sodium phenylbutyrate. Drugs R D 11: 227–249. doi: 10.2165/11591280-000000000-00000 21902286
63. Kang HL, Benzer S, Min KT, (2002) Life extension in Drosophila by feeding a drug. Proc Natl Acad Sci USA 99: 838–843. 11792861