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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

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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PLOS Pathogens


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