Reproductive status alters transcriptomic response to infection in female drosophila melanogaster

G3: Genes, Genomes, Genetics

Volumn 3, Issue 5, 2013, Pages 827-840

  Short, Sarah M ^a,b   Lazzaro, Brian P ^a  

^a Department of Obstetrics Gynecology   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Drosophila melanogaster; Gene expression; Immunity; Microarray; Reproduction

Indexed keywords

MESSENGER RNA; TRANSCRIPTOME;

ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EGG PRODUCTION; ENTEROBACTERIACEAE INFECTION; FEMALE; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; IMMUNITY; MALE; MATING; METABOLISM; MICROARRAY; MICROBIOLOGY; NONHUMAN; OOCYTE; PHYSIOLOGY; PROVIDENCIA; REPRODUCTION; REPRODUCTIVE HEALTH; TRANSCRIPTOMICS; VITELLINE MEMBRANE;

BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER;

EID: 84883256983     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.005306     Document Type: Article

References (48)

1. Agaisse, H., and N. Perrimon, 2004 The roles of JAK/STAT signaling in Drosophila immune responses. Immunol. Rev. 198: 72-82.
2. Agaisse, H., U.-M. Petersen, M. Boutros, B. Mathey-Prevot, and N. Perrimon, 2003 Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev. Cell 5: 441-450.
3. Akam, M. E., and J. R. Carlson, 1985 The detection of Jonah gene transcripts in Drosophila by in situ hybridization. EMBO J. 4: 155-161.
4. Ayres, J. S., and D. S. Schneider, 2009 The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biol. 7: e1000150.
5. Ayres, J. S., N. Freitag, and D. S. Schneider, 2008 Identification of Drosophila mutants altering defense of and endurance to Listeria monocytogenes infection. Genetics 178: 1807-1815.
6. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B. 57: 289-300.
7. Bischoff, V., C. Vignal, I. G. Boneca, T. Michel, J. A. Hoffmann et al., 2004 Function of the Drosophila pattern recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nat. Immunol. 5: 1175-1180.
8. Burke, T., G. L. Waring, E. Popodi, and P. Minoo, 1987 Characterization and sequence of follicle cell genes selectively expressed during vitelline membrane formation in Drosophila. Dev. Biol. 124: 441-450.
9. Carvalho, G. B., P. Kapahi, D. J. Anderson, and S. Benzer, 2006 Allocrine modulation of feeding behavior by the sex peptide of Drosophila. Curr. Biol. 16: 692-696.
10. Cerenius, L., and K. Söderhäll, 2004 The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198: 116-126.
11. Daffre, S., P. Kylsten, C. Samakovlis, and D. Hultmark, 1994 The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract. Mol. Gen. Genet. 242: 152-162.
12. De Gregorio, E., P. T. Spellman, G. M. Rubin, and B. Lemaitre, 2001 Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA 98: 12590- 12595.
13. Eden, E., R. Navon, I. Steinfeld, D. Lipson, and Z. Yakhini, 2009 GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48.
14. Ekengren, S., and D. Hultmark, 2001 A family of Turandot-related genes in the humoral stress response of Drosophila. Biochem. Biophys. Res. Commun. 284: 998-1003.
15. Fedorka, K. M., J. E. Linder, W. Winterhalter, and D. Promislow, 2007 Post-mating disparity between potential and realized immune response in Drosophila melanogaster. Proc. Biol. Sci. 274: 1211-1217.
16. Gigliotti, S., F. Graziani, L. De Ponti, F. Rafti, A. Manzi et al., 1989 Sex, tissue, and stage specific expression of a vitelline membrane protein gene from region 32 of the second chromosome of Drosophila melanogaster. Dev. Genet. 10: 33-41.
17. Heifetz, Y., U. Tram, and M. F. Wolfner, 2001 Male contributions to egg production: the role of accessory gland products and sperm in Drosophila melanogaster. Proc. Biol. Sci. 268: 175-180.
18. Hooper, S. D., S. Boué, R. Krause, L. J. Jensen, C. E. Mason et al., 2007 Identification of tightly regulated groups of genes during Drosophila melanogaster embryogenesis. Mol. Syst. Biol. 3: 72.
19. Innocenti, P., and E. H. Morrow, 2009 Immunogenic males: a genome-wide analysis of reproduction and the cost of mating in Drosophila melanogaster females. J. Evol. Biol. 22: 964-973.
20. Kambris, Z., S. Brun, I.-H. Jang, H.-J. Nam, Y. Romeo 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.
21. Lawniczak, M. K. N., and D. J. Begun, 2004 A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. Genome 47: 900-910.
22. Lazzaro, B. P., and T. J. Little, 2009 Immunity in a variable world. Phil. Trans. R. Soc. B. 364: 15-26.
23. Lemaitre, B., and J. Hoffmann, 2007 The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25: 697-743.
24. Margaritis, L. H., F. C. Kafatos, and W. H. Petri, 1980 The eggshell of Drosophila melanogaster. I. Fine structure of the layers and regions of the wild-type eggshell. J. Cell Sci. 43: 1-35.
25. McGraw, L. A., G. Gibson, A. G. Clark, and M. F. Wolfner, 2004 Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr. Biol. 14: 1509-1514.
26. McGraw, L. A., A. G. Clark, and M. F. Wolfner, 2008 Post-mating gene expression profiles of female Drosophila melanogaster in response to time and to four male accessory gland proteins. Genetics 179: 1395-1408.
27. McKean, K. A., C. Y. Yourth, B. P. Lazzaro, and A. G. Clark, 2008 The evolutionary costs of immunological maintenance and deployment. BMC Evol. Biol. 8: 76.
28. Meunier, N., Y. H. Belgacem, and J. R. Martin, 2007 Regulation of feeding behaviour and locomotor activity by takeout in Drosophila. J. Exp. Biol. 210: 1424-1434.
29. Paredes, J. C., D. P. Welchman, M. Poidevin, and B. Lemaitre, 2011 Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection. Immunity 35: 770-779.
30. Parker, B. J., S. M. Barribeau, A. M. Laughton, J. C. de Roode, and N. M. Gerardo, 2011 Non-immunological defense in an evolutionary framework. Trends Ecol. Evol. 26: 242-248.
31. Pilpel, N., I. Nezer, S. W. Applebaum, and Y. Heifetz, 2008 Matingincreases trypsin in female Drosophila hemolymph. Insect Biochem. Mol. Biol. 38: 320-330.
32. Râberg, L., A. L. Graham, and A. F. Read, 2009 Decomposing health : tolerance and resistance to parasites in animals. Phil. Trans. R. Soc. B 364: 37-49.
33. Ritchie, M. E., J. Silver, A. Oshlack, M. Holmes, D. Diyagama et al., 2007 A comparison of background correction methods for two-colour microarrays. Bioinformatics 23: 2700-2707.
34. Sarov-Blat, L., W. V. So, L. Liu, and M. Rosbash, 2000 The Drosophila takeout gene is a novel molecular link between circadian rythms and feeding behavior. Cell 101: 647-656.
35. Schmid-Hempel, P., 2003 Variation in immune defence as a question of evolutionary ecology. Proc. Biol. Sci. 270: 357-366.
36. Schulenburg, H., J. Kurtz, Y. Moret, and M. T. Siva-Jothy, 2009 Introduction. Ecological immunology. Phil. Trans. R. Soc. B. 364: 3-14.
37. Sheldon, B. C., and S. Verhulst, 1996 Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11: 317-321.
38. Short, S. M., and B. P. Lazzaro, 2010 Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster. Proc. Biol. Sci. 277: 3649-3657.
39. Short, S. M., M. F. Wolfner, and B. P. Lazzaro, 2012 Female Drosophila melanogaster suffer reduced defense against infection due to seminal fluid components. J. Insect Physiol. 58: 1192-1201.
40. Siva-Jothy, M. T., Y. Moret, and J. Rolff, 2005 Insect immunity: an evolutionary ecology perspective. Adv. Ins. Physiol. 32: 1-48.
41. Smyth, G. K., 2005 Limma: linear models for microarray data, pp. 397-420 in Bioinformatics and Computational Biology Solutions Using R and Bioconductor, edited by R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, and W. Huber. Springer, New York.
42. Supek, F., M. Bošnjak, N. Škunca, and T. Šmuc, 2011 REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6: e21800.
43. Tomancak, P., A. Beaton, R. Weiszmann, E. Kwan, S. Shu et al., 2002 Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 3: RESEARCH0088.
44. Tomancak, P., B. P. Berman, A. Beaton, R. Weiszmann, E. Kwan et al., 2007 Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 8: R145.
45. Uttenweiler-Joseph, S., M. Moniatte, M. Lagueux, A. Van Dorsselaer, J. A. Hoffmann et al., 1998 Differential display of peptides induced during the immune response of Drosophila: a matrix-assisted laser desorption ionization time-of-flight mass spectrometry study. Proc. Natl. Acad. Sci. USA 95: 11342-11347.
46. Wang, L., and P. Ligoxygakis, 2006 Pathogen recognition and signalling in the Drosophila innate immune response. Immunobiology 211: 251-261.
47. Wang, X.-H., R. Aliyari, W.-X. Li, H.-W. Li, K. Kim et al., 2006 RNA interference directs innate immunity against viruses in adult Drosophila. Science 312: 452-454.
48. Wang, L., R. J. C. Gilbert, M. L. Atilano, S. R. Filipe, N. J. Gay et al., 2008 Peptidoglycan recognition protein-SD provides versatility of receptor formation in Drosophila immunity. Proc. Natl. Acad. Sci. USA 105: 11881-11886