Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila

PLoS Pathogens

Volumn 9, Issue 10, 2013, Pages

  Regan, Jennifer C ^a,e   Brandão, Ana S ^a,b   Leitão, Alexandre B ^c   Mantas Dias, Ângela Raquel ^a,b   Sucena, Élio ^c,d   Jacinto, António ^a,b   Zaidman Rémy, Anna ^a,b,f  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^d UNIVERSITY OF LISBON   (Portugal)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UA INRA 203   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ECDYSONE; ECDYSONE RECEPTOR; POLYPEPTIDE ANTIBIOTIC AGENT; STEROID HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL INFECTION; BLOOD CELL; CELL MOTILITY; CELL SHAPE; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HORMONAL REGULATION; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; METAMORPHOSIS; MICROARRAY ANALYSIS; NONHUMAN; PECTOBACTERIUM CAROTOVORUM; PHAGOCYTOSIS; POLYMERASE CHAIN REACTION; PUPA (LIFE CYCLE STAGE); RNA ISOLATION; SIGNAL TRANSDUCTION; SURVIVAL; TIME LAPSE IMAGING; TRANSCRIPTOMICS; WOUND;

ANIMALS; BACTERIAL INFECTIONS; DROSOPHILA MELANOGASTER; HEMOCYTES; INSECT HORMONES; LARVA; PHAGOCYTOSIS; SIGNAL TRANSDUCTION; STEROIDS;

EID: 84887276025     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003720     Document Type: Article

References (66)

1. Kollmann TR, Levy O, Montgomery RR, Goriely S, (2012) Innate Immune Function by Toll-like Receptors: Distinct Responses in Newborns and the Elderly. Immunity 37: 771-783.
2. Becker T, Loch G, Beyer M, Zinke I, Aschenbrenner AC, et al. (2010) FOXO-dependent regulation of innate immune homeostasis. Nature 463: 369-373.
3. Cohen S, Janicki-Deverts D, Doyle WJ, Miller GE, Frank E, et al. (2012) Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc Natl Acad Sci U S A 109: 5995-5999.
4. Silver AC, Arjona A, Walker WE, Fikrig E, (2012) The Circadian Clock Controls Toll-like Receptor 9-Mediated Innate and Adaptive Immunity. Immunity 36: 251-261.
5. Stone EF, Fulton BO, Ayres JS, Pham LN, Ziauddin J,et al. The circadian clock protein timeless regulates phagocytosis of bacteria in Drosophila. PLoS Pathog 8: e1002445.
6. Fantuzzi G, Faggioni R, (2000) Leptin in the regulation of immunity, inflammation, and hematopoiesis. J Leukoc Biol 68: 437-446.
7. Gilliver SC, (2010) Sex steroids as inflammatory regulators. J Steroid Biochem Mol Biol 120: 105-115.
8. Lemaitre B, Hoffmann J, (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743.
9. Stuart LM, Boulais J, Charriere GM, Hennessy EJ, Brunet S, et al. (2007) A systems biology analysis of the Drosophila phagosome. Nature 445: 95-101.
10. Stuart LM, Ezekowitz RA, (2008) Phagocytosis and comparative innate immunity: learning on the fly. Nat Rev Immunol 8: 131-141.
11. Avet-Rochex A, Bergeret E, Attree I, Meister M, Fauvarque MO, (2005) Suppression of Drosophila cellular immunity by directed expression of the ExoS toxin GAP domain of Pseudomonas aeruginosa. Cell Microbiol 7: 799-810.
12. 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.
13. Defaye A, Evans I, Crozatier M, Wood W, Lemaitre B, et al. (2009) Genetic ablation of Drosophila phagocytes reveals their contribution to both development and resistance to bacterial infection. J Innate Immun 1: 322-334.
14. Elrod-Erickson M, Mishra S, Schneider D, (2000) Interactions between the cellular and humoral immune responses in Drosophila. Curr Biol 10: 781-784.
15. Kocks C, Cho JH, Nehme N, Ulvila J, Pearson AM, et al. (2005) Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123: 335-346.
16. Matova N, Anderson KV, (2006) Rel/NF-kappaB double mutants reveal that cellular immunity is central to Drosophila host defense. Proc Natl Acad Sci U S A 103: 16424-16429.
17. Nehme NT, Quintin J, Cho JH, Lee J, Lafarge MC, et al. (2011) Relative roles of the cellular and humoral responses in the Drosophila host defense against three gram-positive bacterial infections. PLoS One 6: e14743.
18. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS, (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3: e26.
19. 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.
20. Ulvila J, Vanha-aho LM, Kleino A, Vaha-Makila M, Vuoksio M, et al. (2011) Cofilin regulator 14-3-3zeta is an evolutionarily conserved protein required for phagocytosis and microbial resistance. J Leukoc Biol 89: 649-659.
21. Krzemien J, Crozatier M, Vincent A, (2010) Ontogeny of the Drosophila larval hematopoietic organ, hemocyte homeostasis and the dedicated cellular immune response to parasitism. Int J Dev Biol 54: 1117-1125.
22. Basset A, Khush RS, Braun A, Gardan L, Boccard F, et al. (2000) The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci U S A 97: 3376-3381.
23. Wu SC, Liao CW, Pan RL, Juang JL, (2012) Infection-induced intestinal oxidative stress triggers organ-to-organ immunological communication in Drosophila. Cell Host Microbe 11: 410-417.
24. Babcock DT, Brock AR, Fish GS, Wang Y, Perrin L, et al. (2008) Circulating blood cells function as a surveillance system for damaged tissue in Drosophila larvae. Proc Natl Acad Sci U S A 105: 10017-10022.
25. Stramer B, Wood W, Galko MJ, Redd MJ, Jacinto A, et al. (2005) Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J Cell Biol 168: 567-573.
26. Wood W, Faria C, Jacinto A, (2006) Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster. J Cell Biol 173: 405-416.
27. Bunt S, Hooley C, Hu N, Scahill C, Weavers H, et al. (2010) Hemocyte-secreted type IV collagen enhances BMP signaling to guide renal tubule morphogenesis in Drosophila. Dev Cell 19: 296-306.
28. Olofsson B, Page DT, (2005) Condensation of the central nervous system in embryonic Drosophila is inhibited by blocking hemocyte migration or neural activity. Dev Biol 279: 233-243.
29. DiAngelo JR, Bland ML, Bambina S, Cherry S, Birnbaum MJ, (2009) The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc Natl Acad Sci U S A 106: 20853-20858.
30. Karpac J, Younger A, Jasper H, (2011) Dynamic coordination of innate immune signaling and insulin signaling regulates systemic responses to localized DNA damage. Dev Cell 20: 841-854.
31. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, et al. (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14: 403-414.
32. Thummel CS, (2001) Molecular mechanisms of developmental timing in C. elegans and Drosophila. Dev Cell 1: 453-465.
33. Lanot R, Zachary D, Holder F, Meister M, (2001) Postembryonic hematopoiesis in Drosophila. Dev Biol 230: 243-257.
34. Sampson CJ, Williams MJ, (2012) Real-time analysis of Drosophila post-embryonic haemocyte behaviour. PLoS One 7: e28783.
35. Dimarcq JL, Imler JL, Lanot R, Ezekowitz RA, Hoffmann JA, et al. (1997) Treatment of l(2)mbn Drosophila tumorous blood cells with the steroid hormone ecdysone amplifies the inducibility of antimicrobial peptide gene expression. Insect Biochem Mol Biol 27: 877-886.
36. 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.
37. Zaidman-Remy A, Regan JC, Brandao AS, Jacinto A, (2012) The Drosophila larva as a tool to study gut-associated macrophages: PI3K regulates a discrete hemocyte population at the proventriculus. Dev Comp Immunol 36: 638-647.
38. Franc NC, Dimarcq JL, Lagueux M, Hoffmann J, Ezekowitz RA, (1996) Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4: 431-443.
39. Foley E, O'Farrell PH, (2003) Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Dev 17: 115-125.
40. Bai J, Uehara Y, Montell DJ, (2000) Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103: 1047-1058.
41. Kiger AA, Baum B, Jones S, Jones MR, Coulson A, et al. (2003) A functional genomic analysis of cell morphology using RNA interference. J Biol 2: 27.
42. Rohn JL, Sims D, Liu T, Fedorova M, Schock F, et al. (2011) Comparative RNAi screening identifies a conserved core metazoan actinome by phenotype. J Cell Biol 194: 789-805.
43. Flatt T, Heyland A, Rus F, Porpiglia E, Sherlock C, et al. (2008) Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. J Exp Biol 211: 2712-2724.
44. Zhang Z, Palli SR, (2009) Identification of a cis-regulatory element required for 20-hydroxyecdysone enhancement of antimicrobial peptide gene expression in Drosophila melanogaster. Insect Mol Biol 18: 595-605.
45. Rus F, Flatt T, Tong M, Aggarwal K, Okuda K, et al. (2013) Ecdysone triggered PGRP-LC expression controls Drosophila innate immunity. EMBO J 32: 1626-1638.
46. Harkonen PL, Vaananen HK, (2006) Monocyte-macrophage system as a target for estrogen and selective estrogen receptor modulators. Ann N Y Acad Sci 1089: 218-227.
47. Necela BM, Cidlowski JA, (2004) Mechanisms of glucocorticoid receptor action in noninflammatory and inflammatory cells. Proc Am Thorac Soc 1: 239-246.
48. Dhabhar FS, (2009) Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. Neuroimmunomodulation 16: 300-317.
49. Goulding NJ, (2004) The molecular complexity of glucocorticoid actions in inflammation- a four-ring circus. Curr Opin Pharmacol 4: 629-636.
50. Routley CE, Ashcroft GS, (2009) Effect of estrogen and progesterone on macrophage activation during wound healing. Wound Repair Regen 17: 42-50.
51. Moreira CG, Regan JC, Zaidman-Remy A, Jacinto A, Prag S, (2011) Drosophila hemocyte migration: an in vivo assay for directional cell migration. Methods Mol Biol 769: 249-260.
52. Romeo Y, Lemaitre B, (2008) Drosophila immunity: methods for monitoring the activity of Toll and Imd signaling pathways. Methods Mol Biol 415: 379-394.
53. Kallio MA, Tuimala JT, Hupponen T, Klemela P, Gentile M, et al. (2011) Chipster: user-friendly analysis software for microarray and other high-throughput data. BMC Genomics 12: 507.
54. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
55. Philips JA, Rubin EJ, Perrimon N, (2005) Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309: 1251-1253.
56. Ramet M, Manfruelli P, Pearson A, Mathey-Prevot B, Ezekowitz RA, (2002) Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 416: 644-648.
57. Stroschein-Stevenson SL, Foley E, O'Farrell PH, Johnson AD, (2006) Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol 4: e4.
58. 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.
59. Nonaka S, Nagaosa K, Mori T, Shiratsuchi A, Nakanishi Y, (2013) Integrin alphaPS3/betanu-mediated phagocytosis of apoptotic cells and bacteria in Drosophila. J Biol Chem 288: 10374-10380.
60. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, et al. (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309: 1874-1878.
61. Franc NC, Heitzler P, Ezekowitz RA, White K, (1999) Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284: 1991-1994.
62. Stuart LM, Deng J, Silver JM, Takahashi K, Tseng AA, et al. (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol 170: 477-485.
63. Rahman M, Haberman A, Tracy C, Ray S, Kramer H, (2012) Drosophila mauve mutants reveal a role of LYST homologs late in the maturation of phagosomes and autophagosomes. Traffic 13: 1680-1692.
64. Avet-Rochex A, Perrin J, Bergeret E, Fauvarque MO, (2007) Rac2 is a major actor of Drosophila resistance to Pseudomonas aeruginosa acting in phagocytic cells. Genes Cells 12: 1193-1204.
65. Doherty J, Logan MA, Tasdemir OE, Freeman MR, (2009) Ensheathing glia function as phagocytes in the adult Drosophila brain. J Neurosci 29: 4768-4781.
66. Ziegenfuss JS, Biswas R, Avery MA, Hong K, Sheehan AE, et al. (2008) Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 453: 935-939.