A Critical Role for CLSP2 in the Modulation of Antifungal Immune Response in Mosquitoes
Entomopathogenic fungi represent a promising class of bio-insecticides for mosquito control. Detailed knowledge of molecular mechanisms governing anti-fungal immune response in mosquitoes is essential. CLSP2 composed of serine protease and lectin domains functions as a modulator of the mosquito immune system during the anti-fungal response. Transcriptome analysis indicated that the Toll pathway and melanization genes are highly up-regulated in CLSP2 RNA interference depleted mosquitoes infected with the fungus Beauveria bassiana. A thioester-containing protein TEP22, a member of α2-macroglobulin family, is involved in the CLSP2-modulated mosquito antifungal defense. Our study has contributed to the understanding of immune-modulating mechanisms in mosquitoes.
Vyšlo v časopise:
A Critical Role for CLSP2 in the Modulation of Antifungal Immune Response in Mosquitoes. PLoS Pathog 11(6): e32767. doi:10.1371/journal.ppat.1004931
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004931
Souhrn
Entomopathogenic fungi represent a promising class of bio-insecticides for mosquito control. Detailed knowledge of molecular mechanisms governing anti-fungal immune response in mosquitoes is essential. CLSP2 composed of serine protease and lectin domains functions as a modulator of the mosquito immune system during the anti-fungal response. Transcriptome analysis indicated that the Toll pathway and melanization genes are highly up-regulated in CLSP2 RNA interference depleted mosquitoes infected with the fungus Beauveria bassiana. A thioester-containing protein TEP22, a member of α2-macroglobulin family, is involved in the CLSP2-modulated mosquito antifungal defense. Our study has contributed to the understanding of immune-modulating mechanisms in mosquitoes.
Zdroje
1. Attardo GM, Hansen IA, Raikhel AS (2005) Nutritional regulation of vitellogenesis in mosquitoes: Implications for anautogeny. Insect Biochemistry and Molecular Biology 35: 661–675. 15894184
2. Ramirez JL, Garver LS, Dimopoulos G (2009) Challenges and approaches for mosquito targeted malaria control. Curr Mol Med 9: 116–130. 19275622
3. Fang W, Azimzadeh P, Leger RJ St (2012) Strain improvement of fungal insecticides for controlling insect pests and vector-borne diseases. Curr Opin Microbiol 15: 232–238. doi: 10.1016/j.mib.2011.12.012 22245564
4. Ravetch JV, Lanier LL (2000) Immune inhibitory receptors. Science 290: 84–89. 11021804
5. Ono M, Okada H, Bolland S, Yanagi S, Kurosaki T, et al. (1997) Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell 90: 293–301. 9244303
6. Shin SW, Kokoza V, Bian G, Cheon HM, Kim YJ, et al. (2005) REL1, a homologue of Drosophila dorsal, regulates toll antifungal immune pathway in the female mosquito Aedes aegypti. J Biol Chem 280: 16499–16507. 15722339
7. Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697–743. 17201680
8. Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, et al. (2008) A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 38: 1087–1110. doi: 10.1016/j.ibmb.2008.09.001 18835443
9. Roh KB, Kim CH, Lee H, Kwon HM, Park JW, et al. (2009) Proteolytic cascade for the activation of the insect toll pathway induced by the fungal cell wall component. J Biol Chem 284: 19474–19481. doi: 10.1074/jbc.M109.007419 19473968
10. 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. 17948019
11. 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. 17190605
12. Ligoxygakis P, Pelte N, Hoffmann JA, Reichhart JM (2002) Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 297: 114–116. 12098703
13. 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. 16399077
14. Lemaitre B, Nicolas E, Michaut L, Reichhart J-M, Hoffmann JA (1996) The Dorsoventral Regulatory Gene Cassette spätzle/Toll/cactus Controls the Potent Antifungal Response in Drosophila Adults. Cell 86: 973–983. 8808632
15. Zou Z, Shin SW, Alvarez KS, Kokoza V, Raikhel AS (2010) Distinct melanization pathways in the mosquito Aedes aegypti. Immunity 32: 41–53. doi: 10.1016/j.immuni.2009.11.011 20152169
16. Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS, et al. (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316: 1738–1743. 17588928
17. Kanost MR, Jiang H, Yu XQ (2004) Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 198: 97–105. 15199957
18. Yassine H, Kamareddine L, Osta MA (2012) The mosquito melanization response is implicated in defense against the entomopathogenic fungus Beauveria bassiana. PLoS Pathog 8: e1003029. doi: 10.1371/journal.ppat.1003029 23166497
19. Shin SW, Zou Z, Raikhel AS (2011) A new factor in the Aedes aegypti immune response: CLSP2 modulates melanization. EMBO Rep 12: 938–943. doi: 10.1038/embor.2011.130 21760616
20. Dong Y, Dimopoulos G (2009) Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem 284: 9835–9844. doi: 10.1074/jbc.M807084200 19193639
21. Kokoza V, Ahmed A, Woon Shin S, Okafor N, Zou Z, et al. (2010) Blocking of Plasmodium transmission by cooperative action of Cecropin A and Defensin A in transgenic Aedes aegypti mosquitoes. Proceedings of the National Academy of Sciences 107: 8111–8116. doi: 10.1073/pnas.1003056107 20385844
22. Zou Z, Souza-Neto J, Xi Z, Kokoza V, Shin SW, et al. (2011) Transcriptome analysis of Aedes aegypti transgenic mosquitoes with altered immunity. PLoS Pathog 7: e1002394. doi: 10.1371/journal.ppat.1002394 22114564
23. Fujita T, Matsushita M, Endo Y (2004) The lectin-complement pathway—its role in innate immunity and evolution. Immunol Rev 198: 185–202. 15199963
24. Zhu LL, Zhao XQ, Jiang C, You Y, Chen XP, et al. (2013) C-type lectin receptors Dectin-3 and Dectin-2 form a heterodimeric pattern-recognition receptor for host defense against fungal infection. Immunity 39: 324–334. doi: 10.1016/j.immuni.2013.05.017 23911656
25. Osta MA, Christophides GK, Kafatos FC (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030–2032. 15044804
26. Cheng G, Cox J, Wang P, Krishnan MN, Dai J, et al. (2010) A C-type lectin collaborates with a CD45 phosphatase homolog to facilitate West Nile virus infection of mosquitoes. Cell 142: 714–725. doi: 10.1016/j.cell.2010.07.038 20797779
27. Ji C, Wang Y, Guo X, Hartson S, Jiang H (2004) A pattern recognition serine proteinase triggers the prophenoloxidase activation cascade in the tobacco hornworm, Manduca sexta. J Biol Chem 279: 34101–34106. 15190055
28. Jiang H, Kanost MR (2000) The clip-domain family of serine proteinases in arthropods. Insect Biochem Mol Biol 30: 95–105. 10696585
29. Volohonsky G, Steinert S, Levashina EA (2010) Focusing on complement in the antiparasitic defense of mosquitoes. Trends Parasitol 26: 1–3. doi: 10.1016/j.pt.2009.10.003 19853513
30. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661–670. 15006349
31. Fraiture M, Baxter RH, Steinert S, Chelliah Y, Frolet C, et al. (2009) Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 5: 273–284. doi: 10.1016/j.chom.2009.01.005 19286136
32. Riehle MM, Markianos K, Niare O, Xu J, Li J, et al. (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577–579. 16645095
33. Povelones M, Waterhouse RM, Kafatos FC, Christophides GK (2009) Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324: 258–261. doi: 10.1126/science.1171400 19264986
34. Vasta GR, Quesenberry M, Ahmed H, O'Leary N (1999) C-type lectins and galectins mediate innate and adaptive immune functions: their roles in the complement activation pathway. Dev Comp Immunol 23: 401–420. 10426431
35. Liew FY, Xu D, Brint EK, O'Neill LA (2005) Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 5: 446–458. 15928677
36. Iwami KI, Matsuguchi T, Masuda A, Kikuchi T, Musikacharoen T, et al. (2000) Cutting edge: naturally occurring soluble form of mouse Toll-like receptor 4 inhibits lipopolysaccharide signaling. J Immunol 165: 6682–6686. 11120784
37. De Gregorio E, Spellman PT, Rubin GM, Lemaitre B (2001) Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci U S A 98: 12590–12595. 11606746
38. Hays AR, Raikhel AS (1990) A Novel Protein Produced by the Vitellogenic Fat-Body and Accumulated in Mosquito Oocytes. Rouxs Archives of Developmental Biology 199: 114–121.
39. Xiao G, Ying SH, Zheng P, Wang ZL, Zhang S, et al. (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2: 483. doi: 10.1038/srep00483 22761991
40. Cheon HM, Shin SW, Bian G, Park JH, Raikhel AS (2006) Regulation of lipid metabolism genes, lipid carrier protein lipophorin, and its receptor during immune challenge in the mosquito Aedes aegypti. J Biol Chem 281: 8426–8435. 16449228
41. Yu XQ, Kanost MR (2000) Immulectin-2, a lipopolysaccharide-specific lectin from an insect, Manduca sexta, is induced in response to gram-negative bacteria. J Biol Chem 275: 37373–37381. 10954704
42. Wu TD, Watanabe CK (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859–1875. 15728110
43. Wang L, Feng Z, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136–138. doi: 10.1093/bioinformatics/btp612 19855105
44. Chen X, Hu Y, Zheng H, Cao L, Niu D, et al. (2012) Transcriptome comparison between honey bee queen- and worker-destined larvae. Insect Biochem Mol Biol 42: 665–673. doi: 10.1016/j.ibmb.2012.05.004 22659440
45. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725–2729. doi: 10.1093/molbev/mst197 24132122
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 6
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- HIV Latency Is Established Directly and Early in Both Resting and Activated Primary CD4 T Cells
- A 21st Century Perspective of Poliovirus Replication
- Adenovirus Tales: From the Cell Surface to the Nuclear Pore Complex
- Battling Phages: How Bacteria Defend against Viral Attack