Recovery from an Acute Infection in Requires the GATA Transcription Factor ELT-2

English version České info

Infections by bacterial pathogens often produce substantial tissue damage and alter metabolism in the host that, if left unchecked, could be detrimental to overall fitness. The cellular and systemic responses that resolve these alterations in the host are not well defined. Here, we examine transcriptional networks in an animal host that are modulated during the resolution phase of an intestinal infection treated with an antibiotic. Up-regulation of genes involved in detoxification and cellular homeostasis during the resolution phase is controlled by the conserved endodermal GATA transcription factor ELT-2. GATA transcription factors are known to be involved in the development, differentiation, and function of a diverse array of metazoan tissue types. Therefore, our results ascribe a new role to GATA transcription factors in recovery from an acute infection. Fully characterizing the host response during resolution of an infection will lead to a better understanding of human health concerns related to recurrent infections, wound healing, autoimmune diseases, and chronic inflammatory disorders.

Vyšlo v časopise: Recovery from an Acute Infection in Requires the GATA Transcription Factor ELT-2. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004609
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004609

Souhrn

Zdroje

1. Darby C (2005) Interactions with microbial pathogens. WormBook: 1–15.

2. TenorJL, McCormickBA, AusubelFM, AballayA (2004) Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol 14: 1018–1024.

3. TanMW, RahmeLG, SternbergJA, TompkinsRG, AusubelFM (1999) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96: 2408–2413.

4. GarsinDA, SifriCD, MylonakisE, QinX, SinghKV, et al. (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A 98: 10892–10897.

5. Pukkila-WorleyR, AusubelFM (2012) Immune defense mechanisms in the Caenorhabditis elegans intestinal epithelium. Curr Opin Immunol 24: 3–9.

6. PartridgeFA, Gravato-NobreMJ, HodgkinJ (2010) Signal transduction pathways that function in both development and innate immunity. Dev Dyn 239: 1330–1336.

7. IrazoquiJE, UrbachJM, AusubelFM (2010) Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol 10: 47–58.

8. MeansTK, AballayA (2011) Models to study ancient host-pathogen interactions: lessons from Crete. EMBO reports 12: 5–7.

9. AballayA, YorgeyP, AusubelFM (2000) Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 10: 1539–1542.

10. LeroyM, MosserT, ManiereX, AlvarezDF, MaticI (2012) Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses. BMC evolutionary biology 12: 187.

11. HuangDW, ShermanBT, LempickiRA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols 4: 44–57.

12. KerryS, TeKippeM, GaddisNC, AballayA (2006) GATA transcription factor required for immunity to bacterial and fungal pathogens. PLoS One 1: e77.

13. MalloGV, KurzCL, CouillaultC, PujolN, GranjeaudS, et al. (2002) Inducible antibacterial defense system in C. elegans. Curr Biol 12: 1209–1214.

14. TroemelER, ChuSW, ReinkeV, LeeSS, AusubelFM, et al. (2006) p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2: e183.

15. O'RourkeD, BabanD, DemidovaM, MottR, HodgkinJ (2006) Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res 16: 1005–1016.

16. ShoreDE, RuvkunG (2013) A cytoprotective perspective on longevity regulation. Trends Cell Biol 23: 409–420.

17. XuC, LiCY, KongAN (2005) Induction of phase I, II and III drug metabolism/transport by xenobiotics. Archives of pharmacal research 28: 249–268.

18. ChavezV, Mohri-ShiomiA, GarsinDA (2009) Ce-Duox1/BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect Immun 77: 4983–4989.

19. van der HoevenR, McCallumKC, GarsinDA (2012) Speculations on the activation of ROS generation in C. elegans innate immune signaling. Worm 1: 160–163.

20. SemX, RhenM (2012) Pathogenicity of Salmonella enterica in Caenorhabditis elegans relies on disseminated oxidative stress in the infected host. PLoS One 7: e45417.

21. BurmeisterC, LuersenK, HeinickA, HusseinA, DomagalskiM, et al. (2008) Oxidative stress in Caenorhabditis elegans: protective effects of the Omega class glutathione transferase (GSTO-1). FASEB journal: official publication of the Federation of American Societies for Experimental Biology 22: 343–354.

22. FukushigeT, HawkinsMG, McGheeJD (1998) The GATA-factor elt-2 is essential for formation of the Caenorhabditis elegans intestine. Dev Biol 198: 286–302.

23. McGheeJD, FukushigeT, KrauseMW, MinnemaSE, GoszczynskiB, et al. (2009) ELT-2 is the predominant transcription factor controlling differentiation and function of the C. elegans intestine, from embryo to adult. Dev Biol 327: 551–565.

24. McGheeJD (2013) The Caenorhabditis elegans intestine. Wiley interdisciplinary reviews Developmental biology 2: 347–367.

25. WattsJL (2009) Fat synthesis and adiposity regulation in Caenorhabditis elegans. Trends in endocrinology and metabolism: TEM 20: 58–65.

26. McFall-NgaiM, HadfieldMG, BoschTC, CareyHV, Domazet-LosoT, et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110: 3229–3236.

27. ShaoJ, HeK, WangH, HoWS, RenX, et al. (2013) Collaborative regulation of development but independent control of metabolism by two epidermis-specific transcription factors in Caenorhabditis elegans. The Journal of biological chemistry 288: 33411–33426.

28. ShapiraM, HamlinBJ, RongJ, ChenK, RonenM, et al. (2006) A conserved role for a GATA transcription factor in regulating epithelial innate immune responses. Proc Natl Acad Sci U S A 103: 14086–14091.

29. LeeSH, WongRR, ChinCY, LimTY, EngSA, et al. (2013) Burkholderia pseudomallei suppresses Caenorhabditis elegans immunity by specific degradation of a GATA transcription factor. Proc Natl Acad Sci U S A 110: 15067–15072.

30. KimDH, FeinbaumR, AlloingG, EmersonFE, GarsinDA, et al. (2002) A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297: 623–626.

31. AballayA, DrenkardE, HilbunLR, AusubelFM (2003) Caenorhabditis elegans innate immune response triggered by Salmonella enterica requires intact LPS and is mediated by a MAPK signaling pathway. Curr Biol 13: 47–52.

32. McGhee JD (2007) The C. elegans intestine. WormBook: the online review of C elegans biology: 1–36.

33. McGheeJD, SleumerMC, BilenkyM, WongK, McKaySJ, et al. (2007) The ELT-2 GATA-factor and the global regulation of transcription in the C. elegans intestine. Dev Biol 302: 627–645.

34. ZhangP, JudyM, LeeSJ, KenyonC (2013) 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: 85–100.

35. Glover-CutterKM, LinS, BlackwellTK (2013) Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet 9: e1003701.

36. HoevenR, McCallumKC, CruzMR, GarsinDA (2011) Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog 7: e1002453.

37. RiedelCG, DowenRH, LourencoGF, KirienkoNV, HeimbucherT, et al. (2013) DAF-16 employs the chromatin remodeller SWI/SNF to promote stress resistance and longevity. Nat Cell Biol 15: 491–501.

38. StyerKL, SinghV, MacoskoE, SteeleSE, BargmannCI, et al. (2008) Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science 322: 460–464.

39. SunJ, SinghV, Kajino-SakamotoR, AballayA (2011) Neuronal GPCR controls innate immunity by regulating noncanonical unfolded protein response genes. Science 332: 729–732.

40. ReddyKC, AndersenEC, KruglyakL, KimDH (2009) A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 323: 382–384.

41. SunJ, LiuY, AballayA (2012) Organismal regulation of XBP-1-mediated unfolded protein response during development and immune activation. EMBO reports 13: 855–860.

42. SinghV, AballayA (2012) Endoplasmic reticulum stress pathway required for immune homeostasis is neurally controlled by arrestin-1. The Journal of biological chemistry 287: 33191–33197.

43. AnyanfulA, EasleyKA, BenianGM, KalmanD (2009) Conditioning protects C. elegans from lethal effects of enteropathogenic E. coli by activating genes that regulate lifespan and innate immunity. Cell Host Microbe 5: 450–462.

44. KawliT, TanMW (2008) Neuroendocrine signals modulate the innate immunity of Caenorhabditis elegans through insulin signaling. Nat Immunol 9: 1415–24.

45. EvansEA, KawliT, TanMW (2008) Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin-like signaling pathway in Caenorhabditis elegans. PLoS Pathog 4: e1000175.

46. ZugastiO, EwbankJJ (2009) Neuroimmune regulation of antimicrobial peptide expression by a noncanonical TGF-beta signaling pathway in Caenorhabditis elegans epidermis. Nature immunology 10: 249–256.

47. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.

48. KamathRS, FraserAG, DongY, PoulinG, DurbinR, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231–237.

49. BurtonEA, PendergastAM, AballayA (2006) The Caenorhabditis elegans ABL-1 tyrosine kinase is required for Shigella flexneri pathogenesis. Appl Environ Microbiol 72: 5043–5051.

50. HoisethSK, StockerBA (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238–239.

51. ValdiviaRH, FalkowS (1996) Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22: 367–378.

52. EngelmannI, GriffonA, TichitL, Montanana-SanchisF, WangG, et al. (2011) A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans. PLoS One 6: e19055.