Proteolytic activation and function of the cytokine Spätzle in the innate immune response of a lepidopteran insect, Manduca sexta

FEBS Journal

Volumn 277, Issue 1, 2010, Pages 148-162

  An, Chunju ^a   Jiang, Haobo ^b   Kanost, Michael R ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Antimicrobial peptides; Innate immunity; Manduca sexta; Proteolytic activation; Sp tzle

Indexed keywords

AMINO ACID; ATTACIN 1 PROTEIN; BETA 1,3 GLUCAN; BETA 1,3 GLUCAN RECOGNITION PROTEIN 2; CECROPIN; CECROPIN 6 PROTEIN; COMPLEMENTARY DNA; CYSTINE; CYTOKINE; DISULFIDE; HEMOLIN PROTEIN; HOMODIMER; IMMUNLECTIN 2 PROTEIN; INSECT PROTEIN; LIGAND; LYSOZYME; MORICIN PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEINASE; RECOMBINANT CYTOKINE; SPATZLE PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; GENE INSERTION SEQUENCE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HEMOLYMPH; INJECTION; INNATE IMMUNITY; LARVA; LEPIDOPTERA; MANDUCA SEXTA; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; SILKWORM;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BASE SEQUENCE; BOMBYX; CYTOKINES; DNA, COMPLEMENTARY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION; GENES, INSECT; HEMOLYMPH; IMMUNITY, INNATE; INSECT PROTEINS; MANDUCA; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SERINE PROTEASES; SPECIES SPECIFICITY;

BOMBYX MORI; DROSOPHILA MELANOGASTER; HEXAPODA; MANDUCA SEXTA; NEGIBACTERIA; POSIBACTERIA;

EID: 73649085875     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07465.x     Document Type: Article

References (53)

1. Kanost MR Gorman MJ (2008) Phenoloxidase in insect immunity. In Insect Immunology (Beckage N ed pp. 69 96. Academic Press/Elsevier, San Diego.
2. Cerenius L, Lee BL Soderhall K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29, 263 271.
3. Yu X, Prakash O Kanost MR (2001) Insect ENF family peptides with diverse biological activities display similar core structures in solution. Med Chem Res 10, 493 501.
4. 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.
5. Gillespie JP, Kanost MR Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42, 611 643.
6. Tanji T, Hu X, Weber AN Ip YT (2007) Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol Cell Biol 27, 4578 4588.
7. DeLotto Y DeLotto R (1998) Proteolytic processing of the Drosophila Spatzle protein by easter generates a dimeric NGF-like molecule with ventralising activity. Mech Dev 72, 141 148.
8. DeLotto Y, Smith C DeLotto R (2001) Multiple isoforms of the Drosophila Spatzle protein are encoded by alternatively spliced maternal mRNAs in the precellular blastoderm embryo. Mol Gen Genet 264, 643 652.
9. Weber AN, Tauszig-Delamasure S, Hoffmann JA, Lelievre E, Gascan H, Ray KP, Morse MA, Imler JL Gay NJ (2003) Binding of the Drosophila cytokine Spatzle to Toll is direct and establishes signaling. Nat Immunol 4, 794 800.
10. Hoffmann A, Funkner A, Neumann P, Juhnke S, Walther M, Schierhorn A, Weininger U, Balbach J, Reuter G Stubbs MT (2008) Biophysical characterization of refolded Drosophila Spatzle, a cystine-knot protein, reveals distinct properties of three isoforms. J Biol Chem 283, 32598 32609.
11. Jang IH, Chosa N, Kim SH, Nam HJ, Lemaitre B, Ochiai M, Kambris Z, Brun S, Hashimoto C, Ashida M et al. (2006) A Spatzle-processing enzyme required for toll signaling activation in Drosophila innate immunity. Dev Cell 10, 45 55.
12. Jiang H Kanost MR (2000) The clip-domain family of serine proteinases in arthropods. Insect Biochem Mol Biol 30, 95 105.
13. LeMosy EK, Tan YQ Hashimoto C (2001) Activation of a protease cascade involved in patterning the Drosophila embryo. Proc Natl Acad Sci USA 98, 5055 5060.
14. Hu X, Yagi Y, Tanji T, Zhou S Ip YT (2004) Multimerization and interaction of Toll and Spatzle in Drosophila. Proc Natl Acad Sci USA 101, 9369 9374.
15. Gangloff M, Murali A, Xiong J, Arnot CJ, Weber AN, Sandercock AM, Robinson CV, Sarisky R, Holzenburg A, Kao C et al. (2008) Structural insight into the mechanism of activation of the Toll receptor by the dimeric ligand Spatzle. J Biol Chem 283, 14629 14635.
16. Lemaitre B, Nicolas E, Michaut L, Reichhart JM Hoffmann JA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973 983.
17. Kambris Z, Brun S, Jang IH, Nam HJ, Romeo Y, Takahashi K, Lee WJ, Ueda R Lemaitre B (2006) Drosophila immunity: a large-scale in vivo RNAi screen identifies five serine proteases required for Toll activation. Curr Biol 16, 808 813.
18. Parker JS, Mizuguchi K Gay NJ (2001) A family of proteins related to Spatzle, the toll receptor ligand, are encoded in the Drosophila genome. Proteins 45, 71 80.
19. Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G et al. (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298, 159 165.
20. Shin SW, Bian G Raikhel AS (2006) A toll receptor and a cytokine, Toll5A and Spz1C, are involved in toll antifungal immune signaling in the mosquito Aedes aegypti. J Biol Chem 281, 39388 39395.
21. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z Hultmark D (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15, 645 656.
22. Tribolium Genome Sequencing Consortium, Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Bucher G, Friedrich M et al. (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452, 949 955.
23. Wang Y, Cheng T, Rayaprolu S, Zou Z, Xia Q, Xiang Z Jiang H (2007) Proteolytic activation of pro-spatzle is required for the induced transcription of antimicrobial peptide genes in lepidopteran insects. Dev Comp Immunol 31, 1002 1012.
24. Kim CH, Kim SJ, Kan H, Kwon HM, Roh KB, Jiang R, Yang Y, Park JW, Lee HH, Ha NC et al. (2008) A three-step proteolytic cascade mediates the activation of the peptidoglycan-induced toll pathway in an insect. J Biol Chem 283, 7599 7607.
25. Kan H, Kim CH, Kwon HM, Park JW, Roh KB, Lee H, Park BJ, Zhang R, Zhang J, Soderhall K et al. (2008) Molecular control of phenoloxidase-induced melanin synthesis in an insect. J Biol Chem 283, 25316 25323.
26. Kanost MR, Jiang H Yu XQ (2004) Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 198, 97 105.
27. Ragan EJ, An C, Jiang H Kanost MR (2009) Roles of haemolymph proteins in antimicrobial defences of Manduca sexta. In Insect Infection and Immunity (Rolff J Reynolds SE eds pp. 34 48. Oxford University Press, Oxford.
28. Jiang H (2008) The biochemical basis of antimicrobial responses in Manduca sexta. Insect Sci 15, 53 66.
29. Kanost MR, Dai W Dunn PE (1988) Peptidoglycan fragments elicit antibacterial protein synthesis in larvae of Manduca sexta. Arch Insect Biochem Physiol 8, 147 164.
30. Kanost MR Nardi JB (2009) Innate immune responses of Manduca sexta. In Molecular Biology and Genetics of Lepidoptera (Goldsmith MR Marec F eds pp. 271 291. CRC Press, New York, NY.
31. An C, Ishibashi J, Ragan EJ, Jiang H Kanost MR (2009) Functions of Manduca sexta hemolymph proteinases HP6 and HP8 in two innate immune pathways. J Biol Chem 284, 19716 19726.
32. Zou Z, Najar F, Wang Y, Roe B Jiang H (2008) Pyrosequence analysis of expressed sequence tags for Manduca sexta hemolymph proteins involved in immune responses. Insect Biochem Mol Biol 38, 677 682.
33. 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.
34. Jiang H, Ma C, Lu ZQ Kanost MR (2004) Beta-1,3-glucan recognition protein-2 (betaGRP-2)from Manduca sexta; an acute-phase protein that binds beta-1,3-glucan and lipoteichoic acid to aggregate fungi and bacteria and stimulate prophenoloxidase activation. Insect Biochem Mol Biol 34, 89 100.
35. Ladendorff NE Kanost MR (1991) Bacteria-induced protein P4 (hemolin) from Manduca sexta: a member of the immunoglobulin superfamily which can inhibit hemocyte aggregation. Arch Insect Biochem Physiol 18, 285 300.
36. Morisato D Anderson KV (1995) Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu Rev Genet 29, 371 399.
37. Begun DJ Whitley P (2000) Adaptive evolution of relish, a Drosophila NF-kappaB/IkappaB protein. Genetics 154, 1231 1238.
38. Schlenke TA Begun DJ (2003) Natural selection drives Drosophila immune system evolution. Genetics 164, 1471 1480.
39. Jiggins FM Kim KW (2007) A screen for immunity genes evolving under positive selection in Drosophila. J Evol Biol 20, 965 970.
40. Padgett RA, Grabowski PJ, Konarska MM, Seiler S Sharp PA (1986) Splicing of messenger RNA precursors. Annu Rev Biochem 55, 1119 1150.
41. Kozasa T, Itoh H, Tsukamoto T Kaziro Y (1988) Isolation and characterization of the human Gs alpha gene. Proc Natl Acad Sci USA 85, 2081 2085.
42. Quan F Forte MA (1990) Two forms of Drosophila melanogaster Gs alpha are produced by alternate splicing involving an unusual splice site. Mol Cell Biol 10, 910 917.
43. Irving P, Ubeda JM, Doucet D, Troxler L, Lagueux M, Zachary D, Hoffmann JA, Hetru C Meister M (2005) New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell Microbiol 7, 335 350.
44. De Gregario E, Spellman PT, Rubin GM Lemaitre B (2001) Genome-wide analysis of the Drosophlia immune response by using oligonucleotide microarrays. Proc Natl Acad Sci USA 98, 12590 12595.
45. Ao JQ, Ling E Yu XQ (2008) A Toll receptor from Manduca sexta is in response to Escherichia coli infection. Mol Immunol 45, 543 552.
46. El Chamy L, Leclerc V, Caldelari I Reichhart JM (2008) Sensing of 'danger signals' and pathogen-associated molecular patterns defines binary signaling pathways 'upstream' of Toll. Nat Immunol 9, 1165 1170.
47. Buchon N, Poidevin M, Kwon HM, Guillou A, Sottas V, Lee BL Lemaitre B (2009). A single modular serine protease integrates signals from pattern-recognition receptors upstream of the Drosophila Toll pathway. Proc Natl Acad Sci USA 106, 12442 12447.
48. Dunn PE Drake D (1983) Fate of bacteria injected into naive and immunized larvae of the tobacco hornworm, Manduca sexta. J Invertebr Pathol 41, 77 85.
49. Kapustin Y, Souvorov A, Tatusova T Lipman D (2008) Splign: algorithms for computing spliced alignments with identification of paralogs. Biol Direct 3, 20 32.
50. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389 3402.
51. Kumar S, Tamura K Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5, 150 163.
52. Jiang H, Mulnix AB Kanost MR (1995) Expression and characterization of recombinant Manduca sexta serpin-1B and site-directed mutants that change its inhibitory selectivity. Insect Biochem Mol Biol 25, 1093 1100.
53. Coligan JE, Dunn BM, Ploegh HL, Speicher DW Wingfield PT (1995) Current Protocols in Protein Science pp. 10.5.6 10.5.7. John Wiley & Sons, Inc., Hoboken, NJ.