A Family of CSαβ Defensins and Defensin-Like Peptides from the Migratory Locust, Locusta migratoria, and Their Expression Dynamics during Mycosis and Nosemosis.

Mingyue Lv, Amr Ahmed Mohamed, Liwei Zhang, Pengfei Zhang, Long Zhang
Author Information
  1. Mingyue Lv: Department of Entomology, Key Lab for Biological Control of the Ministry of Agriculture, China Agricultural University, Beijing, P. R. China.
  2. Amr Ahmed Mohamed: Department of Entomology, Faculty of Science, Cairo University, Giza, Egypt.
  3. Liwei Zhang: Department of Entomology, Key Lab for Biological Control of the Ministry of Agriculture, China Agricultural University, Beijing, P. R. China.
  4. Pengfei Zhang: Department of Entomology, Key Lab for Biological Control of the Ministry of Agriculture, China Agricultural University, Beijing, P. R. China.
  5. Long Zhang: Department of Entomology, Key Lab for Biological Control of the Ministry of Agriculture, China Agricultural University, Beijing, P. R. China.

Abstract

Insect defensins are effector components of the innate defense system. During infection, these peptides may play a role in the control of pathogens by providing protective antimicrobial barriers between epithelial cells and the hemocoel. The cDNAs encoding four defensins of the migratory locust, Locusta migratoria, designated LmDEF 1, 3-5, were identified for the first time by transcriptome-targeted analysis. Three of the members of this CSαβ defensin family, LmDEF 1, 3, and 5, were detected in locust tissues. The pro regions of their sequences have little-shared identities with other insect defensins, though the predicted mature peptides align well with other insect defensins. Phylogenetic analysis indicates a completely novel position of both LmDEF 1 and 3, compared to defensins from hymenopterans. The expression patterns of the genes encoding LmDEFs in the fat body and salivary glands were studied in response to immune-challenge by the microsporidian pathogen Nosema locustae and the fungus Metarhizium anisopliae after feeding or topical application, respectively. Focusing on Nosema-induced immunity, qRT-PCR was employed to quantify the transcript levels of LmDEFs. A higher transcript abundance of LmDEF5 was distributed more or less uniformly throughout the fat body along time. A very low baseline transcription of both LmDEFs 1 and 3 in naïve insects was indicated, and that transcription increases with time or is latent in the fat body or salivary glands of infected nymphs. In the salivary glands, expression of LmDEF3 was 20-40-times higher than in the fat body post-microbial infection. A very low expression of LmDEF3 could be detected in the fat body, but eventually increased with time up to a maximum at day 15. Delayed induction of transcription of these peptides in the fat body and salivary glands 5-15 days post-activation and the differential expression patterns suggest that the fat body/salivary glands of this species are active in the immune response against pathogens. The ability of N. locustae to induce salivary glands as well as fat body expression of defensins raises the possibility that these AMPs might play a key role in the development and/or tolerance of parasitic infections.

References

  1. Peptides. 2006 Nov;27(11):2614-23 [PMID: 16914230]
  2. Insect Mol Biol. 2010 Oct;19(5):669-74 [PMID: 20561089]
  3. J Immunol. 2011 Jan 15;186(2):649-56 [PMID: 21209287]
  4. Mini Rev Med Chem. 2006 Jun;6(6):699-709 [PMID: 16787381]
  5. Annu Rev Entomol. 2001;46:667-702 [PMID: 11112183]
  6. Mol Biol Evol. 2000 Jan;17(1):23-31 [PMID: 10666703]
  7. EMBO Rep. 2002 Sep;3(9):852-6 [PMID: 12189180]
  8. Insect Mol Biol. 2004 Feb;13(1):65-72 [PMID: 14728668]
  9. Nucleic Acids Res. 2015 Jan;43(Database issue):D257-60 [PMID: 25300481]
  10. BMC Biol. 2012 May 31;10:47 [PMID: 22651672]
  11. Free Radic Biol Med. 2012 Jun 1-15;52(11-12):2302-11 [PMID: 22542795]
  12. Nat Rev Microbiol. 2008 Jan;6(1):67-78 [PMID: 18079743]
  13. Insect Mol Biol. 2013 Aug;22(4):389-98 [PMID: 23635314]
  14. Adv Appl Microbiol. 2004;54:1-70 [PMID: 15251275]
  15. Insect Mol Biol. 2006 Aug;15(4):393-401 [PMID: 16907826]
  16. J Insect Physiol. 2013 Nov;59(11):1095-103 [PMID: 24013003]
  17. J Insect Physiol. 2012 Aug;58(8):1090-5 [PMID: 22609362]
  18. Annu Rev Entomol. 2005;50:223-45 [PMID: 15355238]
  19. Annu Rev Entomol. 1997;42:611-43 [PMID: 9017902]
  20. Eukaryot Cell. 2005 May;4(5):937-47 [PMID: 15879528]
  21. Peptides. 2007 Jan;28(1):62-75 [PMID: 17161505]
  22. Pharmaceuticals (Basel). 2014 Feb 27;7(3):251-64 [PMID: 24583934]
  23. Annu Rev Microbiol. 2002;56:93-116 [PMID: 12142484]
  24. Cell Mol Life Sci. 2008 Jul;65(13):2069-79 [PMID: 18360739]
  25. Eur J Immunol. 2010 May;40(5):1244-54 [PMID: 20201042]
  26. BMC Genomics. 2010 Mar 19;11:187 [PMID: 20302637]
  27. Nat Protoc. 2008;3(6):1101-8 [PMID: 18546601]
  28. Mol Biol Evol. 2013 Dec;30(12):2725-9 [PMID: 24132122]
  29. Genetics. 2009 Feb;181(2):721-36 [PMID: 19033155]
  30. J Biol Chem. 2004 Feb 6;279(6):4981-7 [PMID: 14630928]
  31. Glycobiology. 2005 Sep;15(9):874-86 [PMID: 15843594]
  32. Insect Biochem Mol Biol. 2008 Dec;38(12):1087-110 [PMID: 18835443]
  33. Dev Comp Immunol. 2016 May;58:102-18 [PMID: 26695127]
  34. J Biol Chem. 2004 May 14;279(20):21121-7 [PMID: 14985331]
  35. Appl Microbiol Biotechnol. 2014 Jul;98(13):5807-22 [PMID: 24811407]
  36. Brief Funct Genomics. 2015 Nov;14(6):407-12 [PMID: 25750410]
  37. Immunol Rev. 2004 Apr;198:169-84 [PMID: 15199962]
  38. Insect Mol Biol. 2000 Oct;9(5):481-90 [PMID: 11029666]
  39. PLoS One. 2015 Mar 26;10(3):e0121884 [PMID: 25811182]
  40. Eur J Biochem. 1992 Nov 1;209(3):977-84 [PMID: 1425705]
  41. BMC Genomics. 2015 Oct 26;16:867 [PMID: 26503342]
  42. FEMS Microbiol Lett. 2002 Jan 2;206(1):9-18 [PMID: 11786250]
  43. EMBO J. 1998 Aug 10;17(5):1217-27 [PMID: 9482719]
  44. Mol Biol Rep. 2009 Apr;36(4):711-6 [PMID: 18360778]
  45. J Biol Chem. 2004 Feb 6;279(6):3900-5 [PMID: 14604982]
  46. Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W89-93 [PMID: 15980588]
  47. Trends Genet. 2005 Jun;21(6):330-2 [PMID: 15922831]
  48. BMC Genomics. 2006 Jan 21;7:11 [PMID: 16426458]
  49. Structure. 1995 May 15;3(5):435-48 [PMID: 7663941]
  50. Glycobiology. 2007 Jan;17(1):56-67 [PMID: 16980327]
  51. J Biol Chem. 1993 Sep 15;268(26):19239-45 [PMID: 7690029]
  52. Insect Biochem Mol Biol. 2001 Feb;31(2):129-37 [PMID: 11164335]
  53. Parasit Vectors. 2015 Feb 04;8:71 [PMID: 25649358]
  54. Environ Microbiol. 2009 Sep;11(9):2284-90 [PMID: 19737304]
  55. Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14614-9 [PMID: 9405661]
  56. Proteins. 2008 Jul;72(1):229-39 [PMID: 18214975]
  57. Eur J Biochem. 1982 Sep;127(1):207-17 [PMID: 7140755]
  58. Protein Pept Lett. 2005 Jan;12(1):3-11 [PMID: 15638797]
  59. PLoS Pathog. 2013 Jan;9(1):e1003102 [PMID: 23326229]
  60. J Biol Chem. 2004 Aug 13;279(33):34562-9 [PMID: 15178692]
  61. J Insect Physiol. 2000 Apr;46(4):429-437 [PMID: 12770206]
  62. Infect Immun. 2004 Dec;72(12):7140-6 [PMID: 15557638]
  63. Curr Top Med Chem. 2015;16(2):206-19 [PMID: 26126908]
  64. Dev Comp Immunol. 2016 Aug;61:60-9 [PMID: 26997372]
  65. Nat Rev Immunol. 2007 Nov;7(11):862-74 [PMID: 17948019]
  66. Biochem J. 1994 Mar 15;298 Pt 3:623-8 [PMID: 8141776]
  67. Immunol Today. 1992 Oct;13(10):411-5 [PMID: 1418378]
  68. Dev Comp Immunol. 2012 Mar;36(3):602-9 [PMID: 22062247]

MeSH Term

Amino Acid Sequence
Animals
Computational Biology
Defensins
Gene Expression
Gene Expression Profiling
Host-Pathogen Interactions
Locusta migratoria
Models, Molecular
Organ Specificity
Phylogeny
Protein Conformation
Transcriptome

Chemicals

Defensins

Word Cloud

Created with Highcharts 10.0.0fatbodydefensinsglandsexpressionsalivary1timepeptidesLmDEF3LmDEFstranscriptioninfectionplayrolepathogensencodinglocustLocustamigratoriaanalysisCSαβdetectedinsectwellpatternsresponselocustaetranscripthigherlowLmDEF3InsecteffectorcomponentsinnatedefensesystemmaycontrolprovidingprotectiveantimicrobialbarriersepithelialcellshemocoelcDNAsfourmigratorydesignated3-5identifiedfirsttranscriptome-targetedThreemembersdefensinfamily5tissuesproregionssequenceslittle-sharedidentitiesthoughpredictedmaturealignPhylogeneticindicatescompletelynovelpositioncomparedhymenopteransgenesstudiedimmune-challengemicrosporidianpathogenNosemafungusMetarhiziumanisopliaefeedingtopicalapplicationrespectivelyFocusingNosema-inducedimmunityqRT-PCRemployedquantifylevelsabundanceLmDEF5distributedlessuniformlythroughoutalongbaselinenaïveinsectsindicatedincreaseslatentinfectednymphs20-40-timespost-microbialeventuallyincreasedmaximumday15Delayedinduction5-15dayspost-activationdifferentialsuggestbody/salivaryspeciesactiveimmuneabilityNinduceraisespossibilityAMPsmightkeydevelopmentand/ortoleranceparasiticinfectionsFamilyDefensinsDefensin-LikePeptidesMigratoryLocustExpressionDynamicsMycosisNosemosis

Similar Articles

Cited By