Loss of p24 function in Drosophila melanogaster causes a stress response and increased levels of NF-κB-regulated gene products

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Boltz, Kara A ^a   Carney, Ginger E ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; GAG PROTEIN; GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; STRESS ACTIVATED PROTEIN KINASE; BAISER PROTEIN, DROSOPHILA; CARRIER PROTEIN; DIF PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; ECLAIR PROTEIN, DROSOPHILA; LOGJAM PROTEIN, DROSOPHILA; RELISH PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR;

ABDOMEN; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE MUTATION; HEAD; IN VIVO STUDY; MOLECULAR GENETICS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; STRESS; THORAX; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; FEMALE; GENE; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; METABOLISM; MUTATION; SIGNAL TRANSDUCTION;

DROSOPHILA MELANOGASTER; EUKARYOTA;

ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOPLASMIC RETICULUM; FEMALE; GENE EXPRESSION PROFILING; GENES, INSECT; GENES, MHC CLASS II; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MEMBRANE TRANSPORT PROTEINS; MUTATION; NF-KAPPA B; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 44349131557     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-212     Document Type: Article

References (65)

1. Aridor M Hannon LA Traffic Jams II: An update of diseases of intracellular transport Traffic 2002 3 781-790 10.1034/ j.1600-0854.2002.31103.x 12383344
2. Cobbold C Monaco AP Sivaprasasdarao A Ponnambalam S Aberrant trafficking of transmembrane proteins in human disease Trends Cell Biol 2003 13 639-647 10.1016/j.tcb.2003.10.008 14624842
3. Selkoe DJ Folding proteins in fatal ways Nature 2003 426 900-904 10.1038/ nature02264 14685251
4. Schröder M Kaufman RJ The mammalian unfolded protein response Annu Rev Biochem 2005 74 739-789 10.1146/annurev.biochem.73.011303.074134 15952902
5. Yoshida H ER stress and diseases FEBS J 2007 274 630-658 10.1111/ j.1742-4658.2007.05639.x 17288551
6. Pahl HL Signal transduction from the endoplasmic reticulum to the cell nucleus Physiol Rev 1999 79 683-701 10390516
7. Harding HP Calfon M Urano F Novoa I Ron D Transcriptional and translational control in the mammalian unfolded protein response Annu Rev Cell Dev Biol 2002 18 575-599 10.1146/ annurev.cellbio.18.011402.160624 12142265
8. Kaufman RJ Scheuner D Schröder M Shen X Lee K Liu CY Arnold SM The unfolded protein response in nutrient sensing and differentiation Nat Rev Mol Cell Biol 2002 3 411-421 10.1038/nrm829 12042763
9. Rutkowski DT Kaufman RJ A trip to the ER: Coping with stress Trends Cell Biol 2004 14 20-28 10.1016/j.tcb.2003.11.001 14729177
10. van Anken E Braakman I Endoplasmic reticulum stress and the making of a professional secretory cell Crit Rev Biochem Mol Biol 2005 40 269-283 10.1080/10409230500315352 16257827
11. Ryoo HD Steller H Unfolded protein responses in Drosophila: Why another model can make it fly Cell Cycle 2007 6 7 830-835 17387279
12. Wek RC Cavener DR Translational control and the unfolded protein response Antioxid Redox Signal 2007 9 12 2357-2371 17760508 10.1089/ ars.2007.1764
13. Pahl HL Baeuerle PA The ER-overload response: Activation of NF-κB Trends Biochem Sci 1997 22 63-67 10.1016/S0968-0004(96)10073-6 9048485
14. Hollien J Weissman JS Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response Science 2006 313-104 107 10.1126/ science.1129631 16825573
15. Pomar N Berlanga JJ Campuzano S Hernández G Elias M de Haro C Functional characterization of Drosophila melanogaster PERK eukaryotic initiation factor 2α (eIF2α) kinase Eur J Biochem 2003 270 293-306 10.1046/j.1432-1033.2003.03383.x 12605680
16. Ryoo HD Domingos PM Kang MJ Steller H Unfolded protein response in a Drosophila model for retinal degeneration EMBO J 2006 26 242-252 1782370 17170705 10.1038/sj.emboj.7601477
17. Souid S Lepesant J-A Yanicostas C The xbp-1 gene is essential for development in Drosophila Dev Genes Evol 2007 217 159-167 10.1007/ s00427-006-0124-1 17206451
18. Jiang H-Y Wek SA McGrath BC Scheuner D Kaufman RJ Cavener DR Wek RC Phosphorylation of the α subunit of eukaryotic initiation factor 2 is required for activation of NF-κB in response to diverse cellular stresses Mol Cell Biol 2003 23 5651-5663 166326 12897138 10.1128/MCB.23.16.5651-5663.2003
19. Deng J Lu PD Zhang Y Scheuner D Kaufman RJ Sonenberg N Harding HP Ron D Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2 Mol Cell Biol 2004 24 10161-10168 529034 15542827 10.1128/MCB.24.23.10161-10168.2004
20. Leonardi A Vito P Mauro C Pacifica F Ulianich L Consiglio E Formisano S Di Jeso B Endoplasmic reticulum stress causes thyroglobulin retention in the organelle and triggers activation of nuclear factor-κB via tumor necrosis factor receptor-associated factor 2 Endocrinology 2002 143 2169-2177 10.1210/en.143.6.2169 12021180
21. Xu C Bailly-Maitre B Reed JC Endoplasmic reticulum stress: Cell life and death decisions J Clinical Investigation 2005 10 2656-2664 10.1172/ JCI26373 16200199 1236697
22. Carney GE Bowen NJ p24 proteins, intracellular trafficking, and behavior: Drosophila melanogaster provides insights and opportunities Biol Cell 2004 96 271-278 10.1016/j.biolcel.2004.01.004 15145531
23. Schimmöller F Singer-Krüger B Schröder S Krüger U Barlowe C Riezman H The absence of Emp24p, a component of ER-derived COPII-coated vesicles, causes a defect in transport of selected proteins to the Golgi EMBO J 1995 14 1329-1339 398218 7729411
24. Stamnes MA Craighead MW Hoe ME Lmapen N Geromanos S Tempst P Rothman JE An integral membrane component of coatomer-coated transport vesicles defines a family of proteins involved in budding Proc Natl Acad Sci USA 1995 92 8011-8015 41276 7644530 10.1073/pnas.92.17.8011
25. Belden WJ Barlowe C Erv25p, a component of COPII-coated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport J Biol Chem 1996 271 26939-26946 10.1074/ jbc.271.43.26939 8900179
26. Belden WJ Barlowe C Deletion of yeast p24 genes activates the unfolded protein response Mol Biol Cell 2001 12 957-969 32279 11294899
27. Carney GE Taylor BJ logjam encodes a putative EMP24/GP25 protein that is required for Drosophila oviposition behavior Genetics 2003 164 173-186 1462565 12750330
28. Boltz KA Ellis LL Carney GE Drosophila melanogaster p24 genes have developmental, tissue-specific and sex-specific expression patterns and functions Dev Dyn 2007 236 544-555 10.1002/dvdy.21032 17131401
29. De Gregorio E Spellman PT Rubin GM Lemaitre B Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays Proc Natl Acad Sci USA 2001 98 12590-12595 60098 11606746 10.1073/ pnas.221458698
30. Irving P Troxler L Heuer TS Belvin M Kopczynski C Reichert J-M Hoffman JA Hetru C A genome-wide analysis of immune responses in Drosophila Proc Natl Acad Sci USA 2001 98 15119-15124 64993 11742098 10.1073/ pnas.261573998
31. Boutros M Agaisse H Perrimon N Sequential activation of signaling pathways during innate immune responses in Drosophila Dev Cell 2002 3 711-722 10.1016/S1534-5807(02)00325-8 12431377
32. De Gregorio E Spellman PT Tzou P Rubin GM Lemaitre B The Toll and Imd pathways are the major regulators of the immune response in Drosophila EMBO J 2002 21 2568-2579 126042 12032070 10.1093/emboj/21.11.2568
33. Markstein M Markstein P Markstein V Levine MS Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo Proc Natl Acad Sci USA 2002 99 763-768 117379 11752406 10.1073/pnas.012591199
34. Silverman N Zhou R Erlich RL Hunter M Bernstein E Schneider D Maniatis T Immune activation of NF-κB and JNK requires Drosophila TAK1 J Biol Chem 2003 278 48928-48934 10.1074/jbc.M304802200 14519762
35. Park JM Brady H Ruocco MG Sun H Williams D Lee SJ Kato T Richards N Chan K Mercurio F Karin M Wasserman SA Targeting of TAK1 by the NF-κB protein Relish regulates the JNK-mediated immune response in Drosophila Genes Dev 2004 18 584-594 374239 15037551 10.1101/gad.1168104
36. Dostert C Jouanguy E Irving P Troxler L Galiana-Arnoux D Hetru C Hoffmann JA Imler J-L The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila Nat Immunol 2005 6 946-953 10.1038/ni1237 16086017
37. Vodovar N Vinals M Liehl P Bassert A Degrouard J Spellman P Boccard F Lemaitre B Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species Proc Natl Acad Sci USA 2005 102 11414-1419 1183552 16061818 10.1073/pnas.0502240102
38. Ip YT Reach M Engstrom Y Kadalayil L Cai H Gonzalez-Crespo S Tatei K Levine M Dif, a dorsal-regulated gene that mediates an immune response in Drosophila Cell 1993 75 753-763 10.1016/0092-8674(93)90495-C 8242747
39. Manfruelli P Reichhart JM Steward R Hoffmann JA Letmaitre B A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and Dif EMBO J 1999 18 3380-3391 1171418 10369678 10.1093/emboj/18.12.3380
40. Meng X Khanuja BS Ip YT Toll receptor-mediated Drosophila immune response requires Dif, an NF-κB factor Genes Dev 1999 13 792-797 316597 10197979 10.1101/gad.13.7.792
41. Rutschmann S Jung AC Hetru V Reichhart J-M Hofmann JA Ferrandon D The Rel protein DIF mediates the antifungal but not the antibacterial host defense in Drosophila Immunity 2000 12 569-580 10.1016/ S1074-7613(00)80208-3 10843389
42. Hedengren M Asling B Dushay MS Ando I Ekengren S Wihlborg M Hultmark D Relish, a central factor in the control of humoral but not cellular immunity in Drosophila Mol Cell 1999 4 5 827-837 10619029 10.1016/ S1097-2765(00)80392-5
43. Girardot F Monnier V Tricore H Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster BMC Genomics 2004 5 74 10.1186/1471-2164-5-74 15458575 526417
44. De Smaele E Zazzeroni F Papa S Nguyen DU Jin R Jones J Cong R Franzoso G Induction of gadd45β by NF-κB downregulates pro-apoptotic JNK signaling Nature 2001 414 308-313 10.1038/35104560 11713530
45. Bartoszewski S Luschnig S Desjeux I Grosshans J Nüsslein-Volhard C Drosophila p24 homologues eclair and baiser are necessary for the activity of the maternally expressed Tkv receptor during embryogenesis Mech Dev 2004 121 1259-1273 10.1016/j.mod.2004.05.006 15327786
46. Harding HP Zhang Y Zeng H Novoa I Lu PD Calfon M Sadri N Yun C Popko B Paules R Stojdl DF Bell JC Hettmann T Leiden JM Ron D An integrated stress response regulates amino acid metabolism and resistance to oxidative stress Mol Cell 2003 11 619-633 10.1016/S1097-2765(03)00105-9 12667446
47. Hedengren-Olcott M Olcott MC Mooney DT Ekengren S Geller BL Taylor BJ Differential activation of the NF-κB-like factors Relish and Dif in Drosophila melanogaster by fungi and gram-positive bacteria J Biol Chem 2004 279 21121-21127 10.1074/jbc.M313856200 14985331
48. Hoffmann JA The immune response of Drosophila Nature 2003 426 33-38 10.1038/nature02021 14603309
49. Yoshida H Matsui T Yamamoto A Okada T Mori K XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor Cell 2001 107 881-891 10.1016/ S0092-8674(01)00611-0 11779464
50. Busse MS Arnold CP Towb P Katrivesis J Wasserman SA A kappaB sequence code for pathway-specific innate immune responses EMBO J 2007 26 3826-3835 10.1038/sj.emboj.7601798 17660749
51. Urano F Wang X Bertolotti A Zhang Y Chung P Harding HP Ron D Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 2000 287 664-666 10.1126/ science.287.5453.664 10650002
52. Arch RH Gedrich RW Thompson CB Tumor necrosis factor receptor-associated factors (TRAFs) - a family of adapter proteins that regulates life and death Genes Dev 1998 12 2821-2830 10.1101/gad.12.18.2821 9744859
53. Liu H Su YC Becker E Treisman J Skolnik EY A Drosophila TNF-receptor-associated factor (TRAF) binds the ste20 kinase Misshapen and activates Jun kinase Curr Biol 1999 9 101-4 10.1016/ S0960-9822(99)80023-2 10021364
54. Zapata JM Matsuzawa S Godzik A Leo E Wasserman SA Reed JC The Drosophila tumor necrosis factor receptor-associated factor-1 (DTRAF1) interacts with Pelle and regulates NFkappaB activity J Biol Chem 2000 275 12102-7 10.1074/jbc.275.16.12102 10766844
55. Shen B Liu H Skolnik EY Manley JL Physical and functional interactions between Drosophila TRAF2 and Pelle kinase contribute to Dorsal activation Proc Natl Acad Sci USA 2001 98 8596-601 37481 11447260 10.1073/pnas.141235698
56. Cha GH Cho KS Lee JH Kim M Kim E Park J Lee SB Chung J Discrete functions of TRAF1 and TRAF2 in Drosophila melanogaster mediated by c-Jun N-terminal kinase and NF-kappaB-dependent signaling pathways Mol Cell Biol 2003 23 7982-91 262421 14585960 10.1128/ MCB.23.22.7982-7991.2003
57. Beg AA Endogenous ligands of Toll-like receptors: Implications for regulating inflammatory and immune responses Trends Immunol 2002 23 509-512 10.1016/S1471-4906(02)02317-7 12401394
58. Wallin RPA Lundqvist A Moré SH von Bonin A Kiessling R Ljunggren H-G Heat-shock proteins as activators of the innate immune system Trends Immunol 2002 23 130-135 10.1016/S1471-4906(01)02168-8 11864840
59. Rapp UK Kaufmann SH Glucose-regulated stress proteins and antibacterial immunity Trends Microbiol 2003 11 11 519-526 14607069 10.1016/ j.tim.2003.09.001
60. Monastirioti M Linn JCE White K Characterization of Drosophila Tyramine B-Hydroxylase gene and isolation of mutant flies lacking octopamine J Neurosci 1996 16 3900-3911 8656284
61. Monastirioti M Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster Dev Biol 2003 264 38-49 10.1016/j.ydbio.2003.07.019 14623230
62. Cole SH Carney GE McClung CA Willard SS Taylor BJ Hirsh J Two functional but noncomplementing Drosophila tyrosine decarboxylase genes J Biol Chem 2005 280 14948-14955 10.1074/jbc.M414197200 15691831
63. Lee HG Seong CS Kim YC Davis RL Han K-A Octopamine receptor OAMB is required for ovulation in Drosophila melanogaster Dev Biol 2003 264 179-190 10.1016/j.ydbio.2003.07.018 14623240
64. Li J Wong L Emerging patterns and gene expression data Genome Inform 2001 12 3-13 11791219
65. Carney GE A rapid genome-wide response to Drosophila melanogaster social interactions BMC Genomics 2007 8 288 1999498 17714588 10.1186/ 1471-2164-8-288