Innate immune responses of Drosophila melanogaster are altered by spaceflight

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Marcu, Oana ^a,b   Lera, Matthew P ^a   Sanchez, Max E ^a,e   Levic, Edina ^a,e   Higgins, Laura A ^a,f   Shmygelska, Alena ^a,c   Fahlen, Thomas F ^a,g   Nichol, Helen ^d   Bhattacharya, Sharmila ^a  

^a NASA AMES RESEARCH CENTER   (United States)

^b SETI INSTITUTE   (United States)

^c CARNEGIE MELLON UNIVERSITY   (United States)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

^e Microfluidic Systems Inc   (United States)

^f SAS INSTITUTE INC   (United States)

^g The Clorox Company   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CELL ADHESION MOLECULE; DROSOCIN; LECTIN; LYSOZYME; OPSONIN; PATTERN RECOGNITION RECEPTOR; PEPTIDOGLYCAN RECOGNITION PROTEIN; PEPTIDOGLYCAN RECOGNITION PROTEIN LA; PEPTIDOGLYCAN RECOGNITION PROTEIN LF; PEPTIDOGLYCAN RECOGNITION PROTEIN SA; PEPTIDOGLYCAN RECOGNITION PROTEIN SB1; PEPTIDOGLYCAN RECOGNITION PROTEIN SC2; PLATELET DERIVED GROWTH FACTOR; POLYPEPTIDE ANTIBIOTIC AGENT; SCAVENGER RECEPTOR C; SCAVENGER RECEPTOR C1; SCAVENGER RECEPTOR C4; THIOESTER; THIOESTER CONTAINING PROTEIN 1; THIOESTER CONTAINING PROTEIN 2; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CLEARANCE; BLOOD CELL; CELL ACTIVITY; CELL CULTURE; CELL MATURATION; COLONY FORMING UNIT; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; FEMALE; GENE FUNCTION; HOST PATHOGEN INTERACTION; HUMORAL IMMUNITY; INNATE IMMUNITY; LARVA; MALE; MICROARRAY ANALYSIS; MICROGRAVITY; NONHUMAN; PATTERN RECOGNITION; PHAGOCYTOSIS; PLASMA CELL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SPACE FLIGHT; ANIMAL; ESCHERICHIA COLI INFECTION; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; MICROBIOLOGY; SIGNAL TRANSDUCTION; WEIGHTLESSNESS;

BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER;

ANIMALS; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; GENE EXPRESSION PROFILING; IMMUNITY, INNATE; MALE; SIGNAL TRANSDUCTION; SPACE FLIGHT; WEIGHTLESSNESS;

EID: 79251574946     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015361     Document Type: Article

References (102)

1. Crucian B, Sams C (2009) Immune system dysregulation during spaceflight: clinical risk for exploration-class missions. J Leukoc Biol 86: 1017-1018.
2. Gueguinou N, Huin-Schohn C, Bascove M, Bueb JL, Tschirhart E, et al. (2009) Could spaceflight-associated immune system weakening preclude the expansion of human presence beyond Earth's orbit? J Leukoc Biol 86: 1027-1038.
3. Sonnenfeld G (2005) The immune system in space, including Earth-based benefits of space-based research. Curr Pharm Biotechnol 6: 343-349.
4. Gould CL, Lyte M, Williams J, Mandel AD, Sonnenfeld G (1987) Inhibited interferon-gamma but normal interleukin-3 production from rats flown on the space shuttle. Aviat Space Environ Med 58: 983-986.
5. Berry WD, Murphy JD, Smith BA, Taylor GR, Sonnenfeld G (1991) Effect of microgravity modeling on interferon and interleukin responses in the rat. J Interferon Res 11: 243-249.
6. Kumei Y, Shimokawa H, Katano H, Hara E, Akiyama H, et al. (1996) Microgravity induces prostaglandin E2 and interleukin-6 production in normal rat osteoblasts: role in bone demineralization. J Biotechnol 47: 313-324.
7. Licato LL, Grimm EA (1999) Multiple interleukin-2 signaling pathways differentially regulated by microgravity. Immunopharmacology 44: 273-279.
8. Walther I, Pippia P, Meloni MA, Turrini F, Mannu F, et al. (1998) Simulated microgravity inhibits the genetic expression of interleukin-2 and its receptor in mitogen-activated T lymphocytes. FEBS Lett 436: 115-118.
9. Crucian BE, Stowe RP, Pierson DL, Sams CF (2008) Immune system dysregulation following short- vs long-duration spaceflight. Aviat Space Environ Med 79: 835-843.
10. Shearer WT, Ochs HD, Lee BN, Cohen EN, Reuben JM, et al. (2009) Immune responses in adult female volunteers during the bed-rest model of spaceflight: antibodies and cytokines. J Allergy Clin Immunol 123: 900-905.
11. Aviles H, Belay T, Vance M, Sonnenfeld G (2005) Effects of space flight conditions on the function of the immune system and catecholamine production simulated in a rodent model of hindlimb unloading. Neuroimmunomodulation 12: 173-181.
12. Aviles H, Belay T, Vance M, Sun B, Sonnenfeld G (2004) Active hexose correlated compound enhances the immune function of mice in the hindlimbunloading model of spaceflight conditions. J Appl Physiol 97: 1437-1444.
13. Klaus DM, Howard HN (2006) Antibiotic efficacy and microbial virulence during space flight. Trends Biotechnol 24: 131-136.
14. Husebye H, Halaas O, Stenmark H, Tunheim G, Sandanger O, et al. (2006) Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. Embo J 25: 683-692.
15. Tzou P, De Gregorio E, Lemaitre B (2002) How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr Opin Microbiol 5: 102-110.
16. Evans CJ, Hartenstein V, Banerjee U (2003) Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev Cell 5: 673-690.
17. Brennan CA, Anderson KV (2004) Drosophila: the genetics of innate immune recognition and response. Annu Rev Immunol 22: 457-483.
18. Franc NC (2002) Phagocytosis of apoptotic cells in mammals, caenorhabditis elegans and Drosophila melanogaster: molecular mechanisms and physiological consequences. Front Biosci 7: d1298-1313.
19. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA (1999) Phylogenetic perspectives in innate immunity. Science 284: 1313-1318.
20. Brennan CA, Delaney JR, Schneider DS, Anderson KV (2007) Psidin is required in Drosophila blood cells for both phagocytic degradation and immune activation of the fat body. Curr Biol 17: 67-72.
21. Kurata S (2010) Extracellular and intracellular pathogen recognition by Drosophila PGRP-LE and PGRP-LC. Int Immunol 22: 143-148.
22. Sackton TB, Lazzaro BP, Clark AG (2010) Genotype and gene expression associations with immune function in Drosophila. PLoS Genet 6: e1000797.
23. 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.
24. Williams MJ (2007) Drosophila hemopoiesis and cellular immunity. J Immunol 178: 4711-4716.
25. Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32: 1295-1309.
26. Cherry S, Silverman N (2006) Host-pathogen interactions in drosophila: new tricks from an old friend. Nat Immunol 7: 911-917.
27. De Gregorio E, Han SJ, Lee WJ, Baek MJ, Osaki T, et al. (2002) An immuneresponsive Serpin regulates the melanization cascade in Drosophila. Dev Cell 3: 581-592.
28. Ferrandon D, Imler JL, Hetru C, Hoffmann JA (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7: 862-874.
29. Lemaitre B, Reichhart JM, Hoffmann JA (1997) Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 94: 14614-14619.
30. Nehme, NT, Liegeois S, Kele B, Giammarinaro P, et al. (2007) A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog 3: e173.
31. Uvell H, Engstrom Y (2007) A multilayered defense against infection: combinatorial control of insect immune genes. Trends Genet 23: 342-349.
32. Becker T, Loch G, Beyer M, Zinke I, Aschenbrenner AC, et al. (2010) FOXOdependent regulation of innate immune homeostasis. Nature 463: 369-373.
33. Lemaitre B, Kromer-Metzger E, Michaut L, Nicolas E, Meister M, et al. (1995) A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci USA 92: 9465-9469.
34. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B (2002) The Toll and Imd pathways are the major regulators of the immune response in Drosophila. Embo J 21: 2568-2579.
35. Levashina EA, Ohresser S, Lemaitre B, Imler JL (1998) Two distinct pathways can control expression of the gene encoding the Drosophila antimicrobial peptide metchnikowin. J Mol Biol 278: 515-527.
36. Khush RS, Leulier F, Lemaitre B (2001) Drosophila immunity: two paths to NF-kappaB. Trends Immunol 22: 260-264.
37. Costa A, Jan E, Sarnow P, Schneider D (2009) The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS One 4: e7436.
38. Delaney JR, Stoven S, Uvell H, Anderson KV, Engstrom Y, et al. (2006) Cooperative control of Drosophila immune responses by the JNK and NFkappaB signaling pathways. Embo J 25: 3068-3077.
39. Bina S, Wright VM, Fisher KH, Milo M, Zeidler MP (2010) Transcriptional targets of Drosophila JAK/STAT pathway signalling as effectors of haematopoietic tumour formation. EMBO Rep 11: 201-207.
40. Agaisse H, Perrimon N (2004) The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev 198: 72-82.
41. Tepass U, Fessler LI, Aziz A, Hartenstein V (1994) Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120: 1829-1837.
42. Holz A, Bossinger B, Strasser T, Janning W, Klapper R (2003) The two origins of hemocytes in Drosophila. Development 130: 4955-4962.
43. Jung SH, Evans CJ, Uemura C, Banerjee U (2005) The Drosophila lymph gland as a developmental model of hematopoiesis. Development 132: 2521-2533.
44. Kurucz E, Vaczi B, Markus R, Laurinyecz B, Vilmos P, et al. (2007) Definition of Drosophila hemocyte subsets by cell-type specific antigens. Acta Biol Hung 58(Suppl): 95-111.
45. Lanot R, Zachary D, Holder F, Meister M (2001) Postembryonic hematopoiesis in Drosophila. Dev Biol 230: 243-257.
46. Wood W, Jacinto A (2007) Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat Rev Mol Cell Biol 8: 542-551.
47. Markus R, Laurinyecz B, Kurucz E, Honti V, Bajusz I, et al. (2009) Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc Natl Acad Sci USA 106: 4805-4809.
48. Irving P, Ubeda JM, Doucet D, Troxler L, Lagueux M, et al. (2005) New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell Microbiol 7: 335-350.
49. Knibiehler B, Mirre C, Cecchini JP, Le Parco Y (1987) Haemocytes accumulate collagen transcripts during Drosophila melanogaster metamorphosis. Roux's Archives of Developmental Biology 196: 243-247.
50. Yasothornsrikul S, Davis WJ, Cramer G, Kimbrell DA, Dearolf CR (1997) Viking: identification and characterization of a second type IV collagen in Drosophila. Gene 198: 17-25.
51. Alfonso T, Jones B (2002) Gcm2 promotes glial cell differentiation and is required with glial cells missing for macrophage development in Drosophila. Developmental Biology 248: 369-383.
52. Krzemien J, Dubois L, Makki R, Meister M, Vincent A, et al. (2007) Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446: 325-328.
53. Kurucz E, Zettervall CJ, Sinka R, Vilmos P, Pivarcsi A, et al. (2003) Hemese, a hemocyte-specific transmembrane protein, affects the cellular immune response in Drosophila. Proc Natl Acad Sci USA 100: 2622-2627.
54. Tokusumi T, Sorrentino RP, Russell M, Ferrarese R, Govind S, et al. (2009) Characterization of a lamellocyte transcriptional enhancer located within the misshapen gene of Drosophila melanogaster. PLoS One 4: e6429.
55. Munier AI, Doucet D, Perrodou E, Zachary D, Meister M, et al. (2002) PVF2, a PDGF/VEGF-like growth factor, induces hemocyte proliferation in Drosophila larvae. EMBO Rep 3: 1195-1200.
56. Pearson A, Lux A, Krieger M (1995) Expression cloning of dSR-CI, a class C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc Natl Acad Sci USA 92: 4056-4060.
57. Ramet M, Pearson A, Manfruelli P, Li X, Koziel H, et al. (2001) Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15: 1027-1038.
58. 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.
59. Tanji T, Ohashi-Kobayashi A, Natori S (2006) Participation of a galactosespecific C-type lectin in Drosophila immunity. The Biochemical Journal 396: 127-138.
60. Lazzaro BP (2008) Natural selection on the Drosophila antimicrobial immune system. Curr Opin Microbiol 11: 284-289.
61. Lagueux M, Perrodou E, Levashina EA, Capovilla M, Hoffmann JA (2000) Constitutive expression of a complement-like protein in toll and JAK gain-offunction mutants of Drosophila. Proc Natl Acad Sci USA 97: 11427-11432.
62. 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.
63. 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.
64. Franc NC, Heitzler P, Ezekowitz RA, White K (1999) Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284: 1991-1994.
65. 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.
66. 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.
67. Leulier F, Parquet C, Pili-Floury S, Ryu J, Caroff M, et al. (2003) The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nature Immunol 4: 478-484.
68. Persson C, Oldenvi S, Steiner H (2007) Peptidoglycan recognition protein LF: A negative regulator of Drosophila immunity. Insect Biochemistry and Molecular Biology 37: 1309-1316.
69. Steiner H (2004) Peptidoglycan recognition proteins: on and off switches for innate immunity. Immunological Reviews. pp 83-96.
70. Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, et al. (2006) Downregulation of the Drosophila immune response by peptidoglycanrecognition proteins SC1 and SC2. PLoS Pathog 2: e14.
71. Jang IH, Chosa N, Kim SH, Nam HJ, Lemaitre B, et al. (2006) A Spatzleprocessing enzyme required for toll signaling activation in Drosophila innate immunity. Developmental Cell 10: 45-55.
72. 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.
73. Kylsten P, Kimbrell DA, Daffre S, Samakovlis C, Hultmark D (1992) The lysozyme locus in Drosophila melanogaster: different genes are expressed in midgut and salivary glands. Mol Gen Genet 232: 335-343.
74. Ekengren S, Hultmark D (2001) A family of turandot-related genes in the humoral stress response of Drosophila. Biochemical and Biophysical Research Communications 284: 998-1003.
75. Ekengren S, Tryselius Y, Dushay MS, Liu G, Steiner H, et al. (2001) A humoral stress response in Drosophila. 11: 714-718.
76. Bernal A, Kimbrell DA (2000) Drosophila Thor participates in host immune defense and connects a translational regulator with innate immunity. Proceedings of the National Academy of Sciences of the United States of America 97: 6019-6024.
77. Busse MS, Arnold CP, Towb P, Katrivesis J, Wasserman SA (2007) A kappaB sequence code for pathway-specific innate immune responses. Embo J 26: 3826-3835.
78. Armstrong JW, Gerren RA, Chapes SK (1995) The effect of space and parabolic flight on macrophage hematopoiesis and function. Exp Cell Res 216: 160-168.
79. Congdon CC, Allebban Z, Gibson LA, Kaplansky A, Strickland KM, et al. (1996) Lymphatic tissue changes in rats flown on Spacelab Life Sciences-2. J Appl Physiol 81: 172-177.
80. Stowe RP, Sams CF, Mehta SK, Kaur I, Jones ML, et al. (1999) Leukocyte subsets and neutrophil function after short-term spaceflight. J Leukoc Biol 65: 179-186.
81. Crucian BE, Cubbage ML, Sams CF (2000) Altered cytokine production by specific human peripheral blood cell subsets immediately following space flight. J Interferon Cytokine Res 20: 547-556.
82. Stowe RP, Sams CF, Pierson DL (2003) Effects of mission duration on neuroimmune responses in astronauts. Aviat Space Environ Med 74: 1281-1284.
83. Taylor GR, Neale LS, Dardano JR (1986) Immunological analyses of U.S. Space Shuttle crewmembers. Aviat Space Environ Med 57: 213-217.
84. Gottar M, Gobert V, Matskevich AA, Reichhart JM, Wang C, et al. (2006) Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127: 1425-1437.
85. Buchon N, Poidevin M, Kwon HM, Guillou A, Sottas V, et al. (2009) A single modular serine protease integrates signals from pattern-recognition receptors upstream of the Drosophila Toll pathway. Proceedings of the National Academy of Sciences of the United States of America 106: 12442-12447.
86. Maillet F, Bischoff V, Vignal C, Hoffmann J, Royet J (2008) The Drosophila peptidoglycan recognition protein PGRP-LF blocks PGRP-LC and IMD/JNK pathway activation. Cell Host Microbe 3: 293-303.
87. Werner T, Liu G, Kang D, Ekengren S, Steiner H, et al. (2000) A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci USA 97: 13772-13777.
88. Liberati NT, Fitzgerald KA, Kim DH, Feinbaum R, Golenbock DT, et al. (2004) Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc Natl Acad Sci USA 101: 6593-6598.
89. Daffre S, Kylsten P, Samakovlis C, Hultmark D (1994) The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract. Mol Gen Genet 242: 152-162.
90. Brun S, Vidal S, Spellman P, Takahashi K, Tricoire H, et al. (2006) The MAPKKK Mekk1 regulates the expression of Turandot stress genes in response to septic injury in Drosophila. Genes Cells 11: 397-407.
91. De Gregorio E, Spellman P T, Rubin G M, Lemaitre B (2001) Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci USA 98: 12590-12595.
92. 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 USA 106: 9797-9802.
93. 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.
94. Marco R, Benguria A, Sanchez J, de Juan E (1996) Effects of the space environment on Drosophila melanogaster development. Implications of the IML-2 experiment. J Biotechnol 47: 179-189.
95. Vernos I, Gonzalez-Jurado J, Calleja M, Marco R (1989) Microgravity effects on the oogenesis and development of embryos of Drosophila melanogaster laid in the Spaceshuttle during the Biorack experiment (ESA). Int J Dev Biol 33: 213-226.
96. Fahlen TF, Sanchez M, Lera M, Blazevic E, Chang J, Bhattacharya, S (2006) A Study of the Effects of Space Flight on the Immune Response in Drosophila Melanogaster. Gravitational and Space Biology 19: 133-134.
97. Qiu P, Pan PC, Govind S (1998) A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125: 1909-1920.
98. 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.
99. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
100. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
101. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B 57: 289-300.
102. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.