Role for sumoylation in systemic inflammation and immune homeostasis in Drosophila larvae

PLoS Pathogens

Volumn 6, Issue 12, 2010, Pages

  Paddibhatla, Indira ^a   Lee, Mark J ^a   Kalamarz, Marta E ^a   Ferrarese, Roberto ^a   Govind, Shubha ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSECT PROTEIN; PROTEIN CACTUS; PROTEIN SPAETZLE; PROTEIN UBC9; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ARTICLE; BLOOD CELL; CHRONIC INFLAMMATION; DROSOPHILA; GENETIC TRANSCRIPTION; HOMEOSTASIS; HUMORAL IMMUNITY; IMMUNOGENETICS; INNATE IMMUNITY; LARVA; NONHUMAN; PARASITOSIS; PROTEIN ANALYSIS; PROTEIN FUNCTION; SUMOYLATION; WASP; ANIMAL; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; INFLAMMATION; PARASITOLOGY;

CACTACEAE; HEXAPODA; VESPOIDEA;

ANIMALS; DROSOPHILA; HOMEOSTASIS; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; INFLAMMATION; LARVA; NF-KAPPA B; SUMOYLATION; TRANSCRIPTION, GENETIC; WASPS;

EID: 78651233297     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001234     Document Type: Article

References (56)

1. Govind S (2008) Innate immunity in Drosophila: Pathogens and pathways. Insect Science 15: 29-43.
2. Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743.
3. Sorrentino RP, Carton Y, Govind S (2002) Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. Dev Biol 243: 65-80.
4. Lee MJ, Kalamarz ME, Paddibhatla I, Small C, Rajwani R, et al. (2009) Virulence factors and strategies of Leptopilina spp.: selective responses in Drosophila hosts. Adv Parasitol 70: 123-145.
5. Schlenke TA, Morales J, Govind S, Clark AG (2007) Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanoga-ster. PLoS Pathog 3: 1486-1501.
6. Peyron P, Vaubourgeix J, Poquet Y, Levillain F, Botanch C, et al. (2008) Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 4: e1000204.
7. Sorrentino RP, Melk JP, Govind S (2004) Genetic analysis of contributions of dorsal group and JAK-Stat92E pathway genes to larval hemocyte concentration and the egg encapsulation response in Drosophila. Genetics 166: 1343-1356.
8. Wertheim B, Kraaijeveld AR, Schuster E, Blanc E, Hopkins M, et al. (2005) Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol 6: R94.
9. Karin M, Lawrence T, Nizet V (2006) Innate immunity gone awry: linking microbial infections to chronic inflammation and cancer. Cell 124: 823-835.
10. Medzhitov R (2008) Origin and physiological roles of inflammation. Nature 454: 428-435.
11. Anthony RM, Rutitzky LI, Urban JF, Jr., Stadecker MJ, Gause WC (2007) Protective immune mechanisms in helminth infection. Nat Rev Immunol 7: 975-987.
12. Loza MJ, McCall CE, Li L, Isaacs WB, Xu J, et al. (2007) Assembly of inflammation-related genes for pathway-focused genetic analysis. PLoS One 2: e1035.
13. Mulinari S, Hacker U, Castillejo-Lopez C (2006) Expression and regulation of Spatzle-processing enzyme in Drosophila. FEBS Lett 580: 5406-5410.
14. Jang IH, Chosa N, Kim SH, Nam HJ, Lemaitre B, et al. (2006) A Spatzle- processing enzyme required for toll signaling activation in Drosophila innate immunity. Dev Cell 10: 45-55.
15. Bodian DL, Leung S, Chiu H, Govind S (2004) Cytokines in Drosophila hematopoiesis and cellular immunity. Prog Mol Subcell Biol 34: 27-46.
16. Qiu P, Pan PC, Govind S (1998) A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125: 1909-1920.
17. Chiu H, Ring BC, Sorrentino RP, Kalamarz M, Garza D, et al. (2005) dUbc9 negatively regulates the Toll-NF-kappa B pathways in larval hematopoiesis and drosomycin activation in Drosophila. Dev Biol 288: 60-72.
18. Huang L, Ohsako S, Tanda S (2005) The lesswright mutation activates Relrelated proteins, leading to overproduction of larval hemocytes in Drosophila melanogaster. Dev Biol 280: 407-420.
19. Lemaitre B, Meister M, Govind S, Georgel P, Steward R, et al. (1995) Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J 14: 536-545.
20. Nicolas E, Reichhart JM, Hoffmann JA, Lemaitre B (1998) In vivo regulation of the IkappaB homologue cactus during the immune response of Drosophila. J Biol Chem 273: 10463-10469.
21. Mabb AM, Miyamoto S (2007) SUMO and NF-kappaB ties. Cell Mol Life Sci 64: 1979-1996.
22. Miura K, Jin JB, Hasegawa PM (2007) Sumoylation, a post-translational regulatory process in plants. Curr Opin Plant Biol 10: 495-502.
23. Stulemeijer IJ, Joosten MH (2008) Post-translational modification of host proteins in pathogen-triggered defence signalling in plants. Mol Plant Pathol 9: 545-560.
24. Asha H, Nagy I, Kovacs G, Stetson D, Ando I, et al. (2003) Analysis of Rasinduced overproliferation in Drosophila hemocytes. Genetics 163: 203-215.
25. Fessler LI, Condic ML, Nelson RE, Fessler JH, Fristrom JW (1993) Site-specific cleavage of basement membrane collagen IV during Drosophila metamorphosis. Development 117: 1061-1069.
26. Harrison DA, Binari R, Nahreini TS, Gilman M, Perrimon N (1995) Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J 14: 2857-2865.
27. Cherbas L, Hu X, Zhimulev I, Belyaeva E, Cherbas P (2003) EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130: 271-284.
28. Sinenko SA, Mathey-Prevot B (2004) Increased expression of Drosophila tetraspanin, Tsp68C, suppresses the abnormal proliferation of ytr-deficient and Ras/Raf-activated hemocytes. Oncogene 23: 9120-9128.
29. Govind S (1996) Rel signalling pathway and the melanotic tumour phenotype of Drosophila. Biochem Soc Trans 24: 39-44.
30. Kambris Z, Brun S, Jang IH, Nam HJ, Romeo Y, et al. (2006) Drosophila immunity: a large-scale in vivo RNAi screen identifies five serine proteases required for Toll activation. Curr Biol 16: 808-813.
31. Geisler R, Bergmann A, Hiromi Y, Nusslein-Volhard C (1992) cactus, a gene involved in dorsoventral pattern formation of Drosophila, is related to the I kappa B gene family of vertebrates. Cell 71: 613-621.
32. Bergmann A, Stein D, Geisler R, Hagenmaier S, Schmid B, et al. (1996) A gradient of cytoplasmic Cactus degradation establishes the nuclear localization gradient of the dorsal morphogen in Drosophila. Mech Dev 60: 109-123.
33. Charroux B, Royet J (2010) Drosophila immune response: From systemic antimicrobial peptide production in fat body cells to local defense in the intestinal tract. Fly (Austin) 4: 40-47.
34. Charroux B, Royet J (2009) Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the Drosophila immune response. Proc Natl Acad Sci U S A 106: 9797-9802.
35. Shia AK, Glittenberg M, Thompson G, Weber AN, Reichhart JM, et al. (2009) Toll-dependent antimicrobial responses in Drosophila larval fat body require Spatzle secreted by haemocytes. J Cell Sci 122: 4505-4515.
36. Scott ML, Fujita T, Liou HC, Nolan GP, Baltimore D (1993) The p65 subunit of NF-kappa B regulates I kappa B by two distinct mechanisms. Genes Dev 7:1266-1276.
37. Nie M, Xie Y, Loo JA, Courey AJ (2009) Genetic and proteomic evidence for roles of Drosophila SUMO in cell cycle control, Ras signaling, and early pattern formation. PLoS One 4: e5905.
38. Stielow B, Sapetschnig A, Kruger I, Kunert N, Brehm A, et al. (2008) Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. Mol Cell 29: 742-754.
39. Manfruelli P, Reichhart JM, Steward R, Hoffmann JA, Lemaitre B (1999) mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. EMBO J 18: 3380-3391.
40. Stanley D, Miller J, Tunaz H (2009) Eicosanoid actions in insect immunity. J Innate Immun 1: 282-290.
41. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420: 860-867.
42. Karin M, Greten FR (2005) NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5: 749-759.
43. Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454: 436-444.
44. Bettencourt R, Asha H, Dearolf C, Ip YT (2004) Hemolymph-dependent and independent responses in Drosophila immune tissue. J Cell Biochem 92: 849-863.
45. Hu X, Yagi Y, Tanji T, Zhou S, Ip YT (2004) Multimerization and interaction of Toll and Spatzle in Drosophila. Proc Natl Acad Sci U S A 101: 9369-9374.
46. Bruckner K, Kockel L, Duchek P, Luque CM, Rorth P, et al. (2004) The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev Cell 7: 73-84.
47. Ferrandon D, Jung AC, Criqui M, Lemaitre B, Uttenweiler-Joseph S, et al. (1998) A drosomycin-GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the Toll pathway. EMBO J 17: 1217-1227.
48. Govind S, Whalen AM, Steward R (1992) In vivo self-association of the Drosophila rel-protein dorsal. Proc Natl Acad Sci U S A 89: 7861-7865.
49. Morales J, Chiu H, Oo T, Plaza R, Hoskins S, et al. (2005) Biogenesis, structure, and immune-suppressive effects of virus-like particles of a Drosophila parasitoid, Leptopilina victoriae. J Insect Physiol 51: 181-195.
50. Whalen AM, Steward R (1993) Dissociation of the dorsal-cactus complex and phosphorylation of the dorsal protein correlate with the nuclear localization of dorsal. J Cell Biol 123: 523-534.
51. Brower DL, Wilcox M, Piovant M, Smith RJ, Reger LA (1984) Related cell-surface antigens expressed with positional specificity in Drosophila imaginaldiscs. Proc Natl Acad Sci U S A 81: 7485-7489.
52. Kwon SY, Xiao H, Glover BP, Tjian R, Wu C, et al. (2008) The nucleosome remodeling factor (NURF) regulates genes involved in Drosophila innate immunity. Dev Biol 316: 538-547.
53. Kurucz E, Markus R, Zsamboki J, Folkl-Medzihradszky K, Darula Z, et al. (2007) Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr Biol 17: 649-654.
54. Senger K, Armstrong GW, Rowell WJ, Kwan JM, Markstein M, et al. (2004) Immunity regulatory DNAs share common organizational features in Drosophila. Mol Cell 13: 19-32.
55. Markstein M, Markstein P, Markstein V, Levine MS (2002) Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo. Proc Natl Acad Sci U S A 99: 763-768.
56. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37: D555-559.