Manduca sexta serpin-5 regulates prophenoloxidase activation and the Toll signaling pathway by inhibiting hemolymph proteinase HP6

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 9, 2010, Pages 683-689

  An, Chunju ^a   Kanost, Michael R ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Clip domain proteinase; Hemolymph; Immunity; Prophenoloxidase activation; Serpin; Toll signaling pathway

Indexed keywords

CATECHOL OXIDASE; ENZYME PRECURSOR; INSECT PROTEIN; PEPTIDE HYDROLASE; PRO PHENOLOXIDASE; PRO-PHENOLOXIDASE; PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR; TOLL LIKE RECEPTOR;

ANIMAL; ARTICLE; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; HEMOLYMPH; IMMUNOLOGY; ISOLATION AND PURIFICATION; LARVA; LEPIDOPTERA; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CATECHOL OXIDASE; ENZYME ACTIVATION; ENZYME PRECURSORS; HEMOLYMPH; INSECT PROTEINS; LARVA; MANDUCA; PEPTIDE HYDROLASES; PROTEASE INHIBITORS; SERPINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

BACTERIA (MICROORGANISMS); HEXAPODA; MANDUCA SEXTA;

EID: 77956191984     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.07.001     Document Type: Article

References (51)

1. Abraham E.G., Pinto S.B., Ghosh A., Vanlandingham D.L., Budd A., Higgs S., et al. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc. Natl. Acad. Sci. U.S.A 2005, 102:16327-16332.
2. Ahmad S.T., Sweeney S.T., Lee J.A., Sweeney N.T., Gao F.B. Genetic screen identifies serpin5 as a regulator of the toll pathway and CHMP2B toxicity associated with frontotemporal dementia. Proc. Natl. Acad. Sci. U.S.A 2009, 106:12168-12173.
3. An C., Ishibashi J., Ragan E.J., Jiang H., Kanost M.R. Functions of Manduca sexta hemolymph proteinases HP6 and HP8 in two innate immune pathways. J. Biol. Chem. 2009, 284:19716-19726.
4. An C., Jiang H., Kanost M.R. Proteolytic activation and function of the cytokine Spätzle in the innate immune response of a lepidopteran insect, Manduca sexta. FEBS J. 2010, 277:148-162.
5. Bian G., Shin S.W., Cheon H.M., Kokoza V., Raikhel A.S. Transgenic alteration of Toll immune pathway in the female mosquito Aedes aegypti. Proc. Natl. Acad. Sci. U.S.A 2005, 102:13568-13573.
6. Buchon N., Poidevin M., Kwon H.M., Guillou A., Sottas V., Lee B.L., et al. A single modular serine protease integrates signals from pattern-recognition receptors upstream of the Drosophila Toll pathway. Proc. Natl. Acad. Sci. U.S.A 2009, 106:12442-12447.
7. Cabrita L.D., Irving J.A., Pearce M.C., Whisstock J.C., Bottomley S.P. Aeropin from the extremophile Pyrobaculum aerophilum bypasses the serpin misfolding trap. J. Biol. Chem. 2007, 282:26802-26809.
8. De Gregorio E., Han S.J., Lee W.J., Baek M.J., Osaki T., Kawabata S., et al. An immune-responsive Serpin regulates the melanization cascade in Drosophila. Dev. Cell 2002, 3:581-592.
9. Dunn P.E., Drake D. Fate of bacteria injected into naive and immunized larvae of the tobacco hornworm, Manduca sexta. J. Invertebr. Pathol. 1983, 41:77-85.
10. El Chamy L., Leclerc V., Caldelari I., Reichhart J.M. Sensing of 'danger signals' and pathogen-associated molecular patterns defines binary signaling pathways 'upstream' of Toll. Nat. Immunol. 2008, 9:1165-1170.
11. Ferrandon D., Imler J.L., Hetru C., Hoffmann J.A. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 2007, 7:862-874.
12. Gettins P.G. Serpin structure, mechanism, and function. Chem. Rev. 2002, 102:4751-4804.
13. Gorman M.J., Wang Y., Jiang H., Kanost M.R. Manduca sexta hemolymph proteinase 21 activates prophenoloxidase-activating proteinase 3 in an insect innate immune response proteinase cascade. J. Biol. Chem. 2007, 282:11742-11749.
14. Green C., Levashina E., McKimmie C., Dafforn T., Reichhart J.M., Gubb D. The necrotic gene in Drosophila corresponds to one of a cluster of three serpin transcripts mapping at 43A1.2. Genetics 2000, 156:1117-1127.
15. Gupta S., Wang Y., Jiang H. Manduca sexta prophenoloxidase (proPO) activation requires proPO-activating proteinase (PAP) and serine proteinase homologs (SPHs) simultaneously. Insect Biochem. Mol. Biol. 2005, 35:241-248.
16. Irving J.A., Pike R.N., Lesk A.M., Whisstock J.C. Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res. 2000, 10:1845-1864.
17. Jang I.H., Chosa N., Kim S.H., Nam H.J., Lemaitre B., Ochiai M., et al. A Spätzle-processing enzyme required for toll signaling activation in Drosophila innate immunity. Dev. Cell. 2006, 10:45-55.
18. Jiang H., Wang Y., Kanost M.R. Pro-phenol oxidase activating proteinase from an insect, Manduca sexta: a bacteria-inducible protein similar to Drosophila easter. Proc. Natl. Acad. Sci. U.S.A 1998, 95:12220-12225.
19. Jiang H., Wang Y., Yu X.Q., Zhu Y., Kanost M. Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochem. Mol. Biol. 2003, 33:1049-1060.
20. Jiang H., Wang Y., Gu Y., Guo X., Zou Z., Scholz F., et al. Molecular identification of a bevy of serine proteinases in Manduca sexta hemolymph. Insect Biochem. Mol. Biol. 2005, 35:931-943.
21. Jiang R., Kim E.H., Gong J.H., Kwon H.M., Kim C.H., Ryu K.H., et al. Three pairs of protease-serpin complexes cooperatively regulate the insect innate immune responses. J. Biol. Chem. 2009, 284:35652-35658.
22. Kan H., Kim C.H., Kwon H.M., Park J.W., Roh K.B., Lee H., et al. Molecular control of phenoloxidase-induced melanin synthesis in an insect. J. Biol. Chem. 2008, 283:25316-25323.
23. Kanost M.R., Gorman M.J. Phenoloxidases in insect immunity. Insect Immunity 2008, 69-96. Academic Press, San Diego. N.E. Beckage (Ed.).
24. Kanost M.R. Serine proteinase inhibitors in arthropod immunity. Dev. Comp. Immunol. 1999, 23:291-301.
25. Kanost M.R. Serpins in a Lepidopteran insect, Manduca sexta. Molecular and Cellular Aspects of the Serpinopathies and Disorders in Serpin Activity 2007, 229-241. World Scientific Publishing Co., Hackensack, NJ. G.A. Silverman, D.A. Lomas (Eds.).
26. Kim C.H., Kim S.J., Kan H., Kwon H.M., Roh K.B., Jiang R., et al. A three-step proteolytic cascade mediates the activation of the peptidoglycan-induced toll pathway in an insect. J. Biol. Chem. 2008, 283:7599-7607.
27. Levashina E.A., Langley E., Green C., Gubb D., Ashburner M., Hoffmann J.A., et al. Constitutive activation of toll-mediated antifungal defense in serpin-deficient Drosophila. Science 1999, 285:1917-1919.
28. Ligoxygakis P., Pelte N., Ji C., Leclerc V., Duvic B., Belvin M., et al. A serpin mutant links Toll activation to melanization in the host defence of Drosophila. EMBO J. 2002, 21:6330-6337.
29. Liu H., Jiravanichpaisal P., Cerenius L., Lee B.L., Soderhall I., Soderhall K. Phenoloxidase is an important component of the defense against Aeromonas hydrophila infection in a crustacean, Pacifastacus leniusculus. J. Biol. Chem. 2007, 282:33593-33598.
30. Michel K., Budd A., Pinto S., Gibson T.J., Kafatos F.C. Anopheles gambiae SRPN2 facilitates midgut invasion by the malaria parasite Plasmodium berghei. EMBO Rep. 2005, 6:891-897.
31. Michel K., Suwanchaichinda C., Morlais I., Lambrechts L., Cohuet A., Awono-Ambene P.H., et al. Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A 2006, 103:16858-16863.
32. Potempa J., Korzus E., Travis J. The serpin superfamily of proteinase inhibitors: structure, function, and regulation. J. Biol. Chem. 1994, 269:15957-15960.
33. Robertson A.S., Belorgey D., Lilley K.S., Lomas D.A., Gubb D., Dafforn T.R. Characterization of the necrotic protein that regulates the Toll-mediated immune response in Drosophila. J. Biol. Chem. 2003, 278:6175-6180.
34. Roh K.B., Kim C.H., Lee H., Kwon H.M., Park J.W., Ryu J.H., et al. Proteolytic cascade for the activation of the insect toll pathway induced by the fungal cell wall component. J. Biol. Chem. 2009, 284:19474-19481.
35. Scherfer C., Tang H., Kambris Z., Lhocine N., Hashimoto C., Lemaitre B. Drosophila Serpin-28D regulates hemolymph phenoloxidase activity and adult pigmentation. Dev. Biol. 2008, 323:189-196.
36. Shin S.W., Bian G., Raikhel A.S. A toll receptor and a cytokine, Toll5A and Spz1C, are involved in toll antifungal immune signaling in the mosquito Aedes aegypti. J. Biol. Chem. 2006, 281:39388-39395.
37. Silverman G.A., Lomas D.A. Molecular and Cellular Aspects of the Serpinopathies and Disorders in Serpin Activity 2007, World Scientific Publishing Co., Hackensack, NJ.
38. Silverman G.A., Bird P.I., Carrell R.W., Church F.C., Coughlin P.B., Gettins P.G., et al. The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature. J. Biol. Chem. 2001, 276:33293-33296.
39. Tang H., Kambris Z., Lemaitre B., Hashimoto C. A serpin that regulates immune melanization in the respiratory system of Drosophila. Dev. Cell. 2008, 15:617-626.
40. Tong Y., Kanost M.R. Manduca sexta serpin-4 and serpin-5 inhibit the prophenoloxidase activation pathway: cDNA cloning, protein expression, and characterization. J. Biol. Chem. 2005, 280:14923-14931.
41. Tong Y., Jiang H., Kanost M.R. Identification of plasma proteases inhibited by Manduca sexta serpin-4 and serpin-5 and their association with components of the prophenoloxidase activation pathway. J. Biol. Chem. 2005, 280:14932-14942.
42. Wang Y., Jiang H. Prophenoloxidase (proPO) activation in Manduca sexta: an analysis of molecular interactions among proPO, proPO-activating proteinase-3, and a cofactor. Insect Biochem. Mol. Biol. 2004, 34:731-742.
43. Wang Y., Jiang H. Interaction of beta-1,3-glucan with its recognition protein activates hemolymph proteinase 14, an initiation enzyme of the prophenoloxidase activation system in Manduca sexta. J. Biol. Chem. 2006, 281:9271-9278.
44. Wang Y., Jiang H. Reconstitution of a branch of the Manduca sexta prophenoloxidase activation cascade in vitro: snake-like hemolymph proteinase 21 (HP21) cleaved by HP14 activates prophenoloxidase-activating proteinase-2 precursor. Insect Biochem. Mol. Biol. 2007, 37:1015-1025.
45. Wang Y., Cheng T., Rayaprolu S., Zou Z., Xia Q., Xiang Z., et al. Proteolytic activation of pro-spätzle is required for the induced transcription of antimicrobial peptide genes in Lepidopteran insects. Dev. Comp. Immunol. 2007, 31:1002-1012.
46. Whisstock J.C., Bottomley S.P. Molecular gymnastics: serpin structure, folding and misfolding. Curr. Opin. Struct. Biol. 2006, 16:761-768.
47. Yu X.Q., Jiang H., Wang Y., Kanost M.R. Nonproteolytic serine proteinase homologs are involved in prophenoloxidase activation in the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 2003, 33:197-208.
48. Zhu Y., Wang Y., Gorman M.J., Jiang H., Kanost M.R. Manduca sexta serpin-3 regulates prophenoloxidase activation in response to infection by inhibiting prophenoloxidase-activating proteinases. J. Biol. Chem. 2003, 278:46556-46564.
49. Zou Z., Jiang H. Manduca sexta serpin-6 regulates immune serine proteinases PAP-3 and HP8. cDNA cloning, protein expression, inhibition kinetics, and function elucidation. J. Biol. Chem. 2005, 280:14341-14348.
50. Zou Z., Shin S.W., Alvarez K.S., Bian G., Kokoza V., Raikhel A.S. Mosquito RUNX4 in the immune regulation of PPO gene expression and its effect on avian malaria parasite infection. Proc. Natl. Acad. Sci. U.S.A 2008, 105:18454-18459.
51. Zou Z., Shin S.W., Alvarez K.S., Kokoza V., Raikhel A.S. Distinct melanization pathways in the mosquito Aedes aegypti. Immunity 2010, 32:41-53.