Gene discovery and differential expression analysis of humoral immune response elements in female Culicoides sonorensis (Diptera: Ceratopogonidae)

Parasites and Vectors

Volumn 7, Issue 1, 2014, Pages

  Nayduch, Dana ^a   Lee, Matthew B ^a   Saski, Christopher A ^b  

^a GRAIN MARKETING AND PRODUCTION RESEARCH CENTER   (United States)

^b CLEMSON UNIVERSITY   (United States)

Author keywords

Attacin; Biting midge; Cecropin; Defensin; Imd; Innate immunity; JAK STAT; RNAseq; Toll

Indexed keywords

HUMORAL ANTIBODY; JANUS KINASE; MEMBRANE RECEPTOR; MONOPHENOL MONOOXYGENASE; POLYPEPTIDE ANTIBIOTIC AGENT; PROPHENOLOXIDASE; STAT PROTEIN; SUCROSE; THIOESTER; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; INSECT PROTEIN; TRANSCRIPTOME;

ARTICLE; BLOOD; CULICOIDES; CULICOIDES SONORENSIS; DIGESTIVE SYSTEM; FEEDING; GENE EXPRESSION; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; INNATE IMMUNITY; INTESTINE FLORA; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; AMINO ACID SEQUENCE; ANIMAL; CERATOPOGONIDAE; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ANIMALS; CERATOPOGONIDAE; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDIES; IMMUNITY, HUMORAL; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84924095353     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-7-388     Document Type: Article

References (63)

1. Drolet BS, Campbell CL, Stuart MA, Wilson WC: Vector competence of Culicoides sonorensis (Diptera: Ceratopogonidae) for vesicular stomatitis virus. J Med Entomol 2005, 42(3):409-418.
2. Perez De Leon AA, Tabachnick WJ: Transmission of vesicular stomatitis New Jersey virus to cattle by the biting midge Culicoides sonorensis (Diptera: Ceratopogonidae). J Med Entomol 2006, 43(2):323-329.
3. Wigglesworth VB: Digestion and Nutrition. In The Principles of Insect Physiology. &th edition. New York: Chapman and Hall; 1972:476-552.
4. Lemaitre B, Hoffmann J: The host defense of Drosophila melanogaster. Annu Rev Immunol 2007, 25(1):697-743.
5. Gilbert LI: Insect Molecular Biology and Biochemistry. London, UK: Academic Press; 2012.
6. El Chamy L, Leclerc V, Caldelari I, Reichhart JM: Sensing of 'danger signals' and pathogen-associated molecular patterns defines binary signaling pathways 'upstream' of Toll. Nat Immunol 2008, 9(10):1165-1170.
7. 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(9):946-953.
8. Souza-Neto JA, Sim S, Dimopoulos G: An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci USA 2009, 106(42):17841-17846.
9. Xi Z, Ramirez JL, Dimopoulos G: The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 2008, 4(7):e1000098.
10. Kingsolver MB, Huang Z, Hardy RW: Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol 2013, 425(24):4921-4936.
11. Bulet P, Hetru C, Dimarcq JL, Hoffmann D: Antimicrobial peptides in insects: structure and function. Dev Comp Immunol 1999, 23(4-5):329-344.
12. Bulet P, Stöcklin R: Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept Lett 2005, 12(1):3-11.
13. Bulet P, Stöcklin R, Menin L: Antimicrobial peptides: from invertebrates to vertebrates. Immunol Rev 2004, 198(1):169-184.
14. Dimopoulos G, Richman A, Müller HM, Kafatos FC: Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc Natl Acad Sci USA 1997, 94(21):11508-11513.
15. Dimopoulos G, Seeley D, Wolf A, Kafatos FC: Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO J 1998, 17(21):6115-6123.
16. Richman AM, Dimopoulos G, Seeley D, Kafatos FC: Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. EMBO J 1997, 16(20):6114-6119.
17. Boulanger N, Bulet P, Lowenberger C: Antimicrobial peptides in the interactions between insects and flagellate parasites. TRENDS Parasitol 2006, 22(6):262-268.
18. Hao Z, Kasumba I, Lehane MJ, Gibson WC, Kwon J, Aksoy S: Tsetse immune responses and trypanosome transmission: implications for the development of tsetse-based strategies to reduce trypanosomiasis. Proc Natl Acad Sci USA 2001, 98(22):12648-12653.
19. Nayduch D, Aksoy S: Refractoriness in tsetse flies (Diptera: Glossinidae) may be a matter of timing. J Med Entomol 2007, 44(4):660-665.
20. Parker MD, Akey DH, Lauerman LH: Persistence of enterobacteriaceae in female adults of the biting gnat Culicoides variipennis (Diptera: Ceratopogonidae). J Med Entomol 1978, 14(5):597-598.
21. Parker MD, Akey DH, Lauerman LH: Microbial flora associated with colonized and wild populations of the biting gnat Culicoides variipennis. Entomol Exp Appl 1977, 21(2):130-136.
22. Volf P, Kiewegová A, Nemec A: Bacterial colonisation in the gut of Phlebotomus duboscqi (Diptera: Psychodidae): transtadial passage and the role of female diet. Folia Parasitol (Praha) 2002, 49(1):73-77.
23. Peterkova-Koci K, Robles-Murguia M, Ramalho-Ortigao M, Zurek L: Significance of bacteria in oviposition and larval development of the sand fly Lutzomyia longipalpis. Parasit Vectors 2012, 5:145.
24. Demaio J, Pumpuni CB, Kent M, Beier JC: The midgut bacterial flora of wild Aedes triseriatus, Culex pipiens, and Psorophora columbiae mosquitoes. Amer J Trop Med Hyg 1996, 54(2):219-223.
25. Leulier F, Royet J: Maintaining immune homeostasis in fly gut. Nat Immunol 2009, 10(9):936-938.
26. Lhocine N, Ribeiro PS, Buchon N, Wepf A, Wilson R, Tenev T, Lemaitre B, Gstaiger M, Meier P, Leulier F: PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 2008, 4(2):147-158.
27. Ramirez JL, Souza-Neto J, Cosme RT, Rovira J, Ortiz A, Pascale JM, Dimopoulos G: Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Negl Trop Dis 2012, 6(3):e1561.
28. Azambuja P, Garcia ES, Ratcliffe NA: Gut microbiota and parasite transmission by insect vectors. Trends Parasitol 2005, 21(12):568-572.
29. Weiss B, Aksoy S: Microbiome influences on insect host vector competence. Trends Parasitol 2011, 27(11):514-522.
30. Nayduch D, Lee MB, Saski CA: The reference transcriptome of the adult female biting midge (Culicoides sonorensis) and differential gene expression profiling during teneral, blood, and sucrose feeding conditions. PLoS ONE 2014, 9(5):e98123.
31. Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30(9):e36.
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(11):2568-2579.
33. Cooper DM, Chamberlain CM, Lowenberger C: Aedes FADD: a novel death domain-containing protein required for antibacterial immunity in the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol 2009, 39(1):47-54.
34. Aggarwal K, Silverman NS: Positive and negative regulation of the Drosophila immune response. BMB Rep 2008, 41(4):267-277.
35. Lee KZ, Ferrandon D: Negative regulation of immune responses on the fly. EMBO J 2011, 30(6):988-990.
36. Ferrandon D, Imler JL, Hoffmann JA: Sensing infection in Drosophila: toll and beyond. Semin Immunol 2004, 16(1):43-53.
37. Tauszig S, Jouanguy E, Hoffmann JA, Imler JL: Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc Natl Acad Sci USA 2000, 97(19):10520-10525.
38. Imler J-L, Hoffmann JA: Toll receptors in innate immunity. Trends Cell Biol 2001, 11(7):304-311.
39. Li X-C, Zhang X-W, Zhou J-F, Ma H-Y, Liu Z-D, Zhu L, Yao X-J, Li L-G, Fang W-H: Identification, characterization, and functional analysis of tube and pelle homologs in the mud crab Scylla paramamosain. PloS ONE 2013, 8(10):e76728.
40. Towb P, Sun H, Wasserman SA: Tube Is an IRAK-4 homolog in a Toll pathway adapted for development and immunity. J Innate Immun 2009, 1(4):309-321.
41. Shin SW, Kokoza V, Bian G, Cheon H-M, Kim YJ, Raikhel AS: REL1, a homologue of Drosophila dorsal, regulates toll antifungal immune pathway in the female mosquito Aedes aegypti. J Biol Chem 2005, 280(16):16499-16507.
42. Hedengren M, Borge K, Hultmark D: Expression and evolution of the Drosophila attacin/diptericin gene family. Biochem Biophys Res Commun 2000, 279(2):574-581.
43. Cudic M, Bulet P, Hoffmann R, Craik DJ, Otvos L Jr: Chemical synthesis, antibacterial activity and conformation of diptericin, an 82-mer peptide originally isolated from insects. Eur J Biochem 1999, 266(2):549-558.
44. Tossi A, Sandri L, Giangaspero A: Amphipathic, α-helical antimicrobial peptides. Peptide Sci 2000, 55(1):4-30.
45. Imler JL, Bulet P: Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem Immunol Allergy 2005, 86:1-21.
46. Bechinger B: Structure and functions of channel-forming peptides: magainins, cecropins, melittin and alamethicin. J Membr Biol 1997, 156(3):197-211.
47. Rawlings JS, Rosler KM, Harrison DA: The JAK/STAT signaling pathway. J Cell Sci 2004, 117(8):1281-1283.
48. Callus BA, Mathey-Prevot B: SOCS36E, a novel Drosophila SOCS protein, suppresses JAK/STAT and EGF-R signaling in the imaginal wing disc. Oncogene 2002, 21(31):4812-4821.
49. Jackson PK: A new RING for SUMO: wrestling transcriptional responses into nuclear bodies with PIAS family E3 SUMO ligases. Genes Dev 2001, 15(23):3053-3058.
50. Blandin S, Levashina EA: Thioester-containing proteins and insect immunity. Mol Immunol 2004, 40(12):903-908.
51. Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS, Bartholomay LC, Barillas-Mury C, Bian G, Blandin S, Christensen BM: Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007, 316(5832):1738-1743.
52. Oliveira JHM, Gonçalves RL, Lara FA, Dias FA, Gandara ACP, Menna-Barreto RF, Edwards MC, Laurindo FR, Silva-Neto MA, Sorgine MH: Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog 2011, 7(3):e1001320.
53. Pumpuni CB, Demaio J, Kent M, Davis JR, Beier JC: Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am J Trop Med Hyg 1996, 54(2):214-218.
54. Hao Z, Kasumba I, Aksoy S: Proventriculus (cardia) plays a crucial role in immunity in tsetse fly (Diptera: Glossinidiae). Insect Biochem Mol Biol 2003, 33(11):1155-1164.
55. Foley E, O'Farrell PH: Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Dev 2003, 17(1):115-125.
56. Stenbak CR, Ryu JH, Leulier F, Pili-Floury S, Parquet C, Herve M, Chaput C, Boneca IG, Lee WJ, Lemaitre B, Mengin-Lecreulx D: Peptidoglycan molecular requirements allowing detection by the Drosophila immune deficiency pathway. JImmunol2004, 173(12):7339-7348.
57. Gendrin M, Welchman DP, Poidevin M, Hervé M, Lemaitre B: Long-range activation of systemic immunity through peptidoglycan diffusion in Drosophila. PLoS Pathog 2009, 5(12):e1000694.
58. Meister S, Agianian B, Turlure F, Relógio A, Morlais I, Kafatos FC, Christophides GK: Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog 2009, 5(8):e1000542.
59. Garver LS, Bahia AC, Das S, Souza-Neto JA, Shiao J, Dong Y, Dimopoulos G: Anopheles Imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLoS Pathog 2012, 8(6):e1002737.
60. Cirimotich CM, Ramirez JL, Dimopoulos G: Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 2011, 10(4):307-310.
61. Nakajima Y, Taylor D, Yamakawa M: Antibacterial peptide defensin is involved in midgut immunity of the soft tick, Ornithodoros moubata. Insect Mol Biol 2002, 11(6):611-618.
62. Munks R, Hamilton J, Lehane S, Lehane M: Regulation of midgut defensin production in the bloodsucking insect Stomoxys calcitrans. Insect Mol Biol 2001, 10(6):561-571.
63. Lehrer RI, Ganz T: Antimicrobial peptides in mammalian and insect host defence. Curr Opin Immunol 1999, 11(1):23-27.