Protease inhibitors and proteolytic signalling cascades in insects

Enfermedades Infecciosas y Microbiologia Clinica

Volumn 28, Issue SUPPL. 3, 2010, Pages 1749-1759

  Gubb, David ^a   Sanz Parra, Arantza ^a   Barcena, Laura ^a   Troxler, Laurent ^b   Fullaondo, Ane ^a  

^a CIC BIOGUNE   (Spain)

^b INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Insect; Kazal; Protease inhibitors; Serpin; Signalling

Indexed keywords

ALPHA 2 MACROGLOBULIN; APROTININ; CARRIER PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MACROGLOBULIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEINASE; PROTEINASE INHIBITOR; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; TOLL LIKE RECEPTOR; VIRULENCE FACTOR;

ARTICLE; BETA SHEET; DROSOPHILA MELANOGASTER; EMPHYSEMA; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME INHIBITION; HEMOLYMPH; INNATE IMMUNITY; INSECT; NONHUMAN; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; DROSOPHILA; PHYSIOLOGICAL PROCESS; TICK;

HEXAPODA;

EID: 78650236051     PISSN: 0213005X     EISSN: 15781852     Source Type: Journal    
DOI: 10.1016/j.biochi.2010.09.004     Document Type: Review

References (83)

1. D.A. Lomas, D. Belorgey, M. Mallya, E. Miranda, K.J. Kinghorn, L.K. Sharp, R.L. Phillips, R. Page, A.S. Robertson, and D.C. Crowther Molecular mousetraps and the serpinopathies Biochem. Soc. Trans. 33 2005 321 330
2. D.A. Lomas New insights into the structural basis of alpha 1-antitrypsin deficiency Qjm 89 1996 807 812
3. K.M. Providence, and P.J. Higgins PAI-1 expression is required for epithelial cell migration in two distinct phases of in vitro wound repair J. Cell Physiol. 200 2004 297 308
4. N.D. Rawlings, D.P. Tolle, and A.J. Barrett Evolutionary families of peptidase inhibitors Biochem. J. 378 2004 705 716
5. G. Xu, R.L. Rich, C. Steegborn, T. Min, Y. Huang, D.G. Myszka, and H. Wu Mutational analyses of the p35-caspase interaction. A bowstring kinetic model of caspase inhibition by p35 J. Biol. Chem. 278 2003 5455 5461
6. A.J. Barrett Alpha 2-macroglobulin Methods Enzymol. 80 Pt C 1981 737 754
7. L. Sottrup-Jensen Alpha-macroglobulins: structure, shape, and mechanism of proteinase complex formation J. Biol. Chem. 264 1989 11539 11542
8. N.D. Rawlings, F.R. Morton, C.Y. Kok, J. Kong, and A.J. Barrett MEROPS: the peptidase database Nucleic Acids Res. 36 2008 D320 D325
9. L.A. Kazal, D.S. Spicer, and R.A. Brahinsky Isolation of a crystalline trypsin inhibitor-anticoagulant protein from pancreas J. Am. Chem. Soc. 70 1948 3034 3040
10. P.G. Gettins Serpin structure, mechanism, and function Chem. Rev. 102 2002 4751 4804
11. J.A. Huntington, R.J. Read, and R.W. Carrell Structure of a serpin-protease complex shows inhibition by deformation Nature 407 2000 923 926
12. J.A. Irving, R.N. Pike, A.M. Lesk, and J.C. Whisstock Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function Genome Res. 10 2000 1845 1864
13. G.A. Silverman, P.I. Bird, R.W. Carrell, F.C. Church, P.B. Coughlin, P.G. Gettins, J.A. Irving, D.A. Lomas, C.J. Luke, R.W. Moyer, P.A. Pemberton, E. Remold-O'Donnell, G.S. Salvesen, J. Travis, and J.C. Whisstock 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. 276 2001 33293 33296
14. L. Sottrup-Jensen, O. Sand, L. Kristensen, and G.H. Fey The alpha-macroglobulin bait region. Sequence diversity and localization of cleavage sites for proteinases in five mammalian alpha-macroglobulins J. Biol. Chem. 264 1989 15781 15789
15. P.G. Gettins Thiol ester cleavage-dependent conformational change in human alpha 2-macroglobulin. Influence of attacking nucleophile and of Cys949 modification Biochemistry 34 1995 12233 12240
16. P.G. Gettins, B. Crews, A.H. Beth, and K. Hideg Bait region-thiol ester mapping in human alpha 2-macroglobulin FEBS Lett. 367 1995 137 140
17. P.C. Harpel, M.F. Lewin, and A.P. Kaplan Distribution of plasma kallikrein between C-1 inactivator and alpha 2-macroglobulin in plasma utilizing a new assay for alpha 2-macroglobulin-kallikrein complexes J. Biol. Chem. 260 1985 4257 4263
18. M. Kunitz Crystallization of a trypsin inhibitor from soybean Science 101 1945 668 669
19. J. Sri Ram, L. Terminiello, M. Bier, and F.F. Nord On the mechanism of enzyme action.LVII. Interaction between trypsin and ovomucoid Arch. Biochem. Biophys. 52 1954 451 463
20. R.M. Roberts, N. Mathialagan, J.Y. Duffy, and G.W. Smith Regulation and regulatory role of proteinase inhibitors Crit. Rev. Eukaryot. Gene Expr. 5 1995 385 436
21. M. Laskowski, and M.A. Qasim What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes? Biochim. Biophys. Acta 1477 2000 324 337
22. R.J. Beynon, and J.S. Bond Proteolytic Enzymes 1998 IRL at Oxford University press Oxford
23. A. Mulenga, R. Khumthong, and K.C. Chalaire Ixodes scapularis tick serine proteinase inhibitor (serpin) gene family; annotation and transcriptional analysis BMC Genomics 10 2009 217
24. J.M. Reichhart Tip of another iceberg: Drosophila serpins Trends Cell Biol. 15 2005 659 665
25. J. Ross, H. Jiang, M.R. Kanost, and Y. Wang Serine proteases and their homologs in the Drosophila melanogaster genome: an initial analysis of sequence conservation and phylogenetic relationships Gene 304 2003 117 131
26. T.P. Baglin, R.W. Carrell, F.C. Church, C.T. Esmon, and J.A. Huntington Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism Proc. Natl. Acad. Sci. U S A 99 2002 11079 11084
27. M. Garrett, A. Fullaondo, L. Troxler, G. Micklem, and D. Gubb Identification and analysis of serpin-family genes by homology and synteny across the 12 sequenced Drosophilid genomes BMC Genomics 10 2009 489
28. V. Alva, K.K. Koretke, M. Coles, and A.N. Lupas Cradle-loop barrels and the concept of metafolds in protein classification by natural descent Curr. Opin. Struct. Biol. 18 2008 358 365
29. E. De Gregorio, S.J. Han, W.J. Lee, M.J. Baek, T. Osaki, S. Kawabata, B.L. Lee, S. Iwanaga, B. Lemaitre, and P.T. Brey An immune-responsive serpin regulates the melanization cascade in Drosophila Dev. Cell 3 2002 581 592
30. E.A. Levashina, E. Langley, C. Green, D. Gubb, M. Ashburner, J.A. Hoffmann, and J.M. Reichhart Constitutive activation of toll-mediated antifungal defense in serpin-deficient Drosophila Science 285 1999 1917 1919
31. P. Ligoxygakis, N. Pelte, C. Ji, V. Leclerc, B. Duvic, M. Belvin, H. Jiang, J.A. Hoffmann, and J.M. Reichhart A serpin mutant links Toll activation to melanization in the host defence of Drosophila EMBO J. 21 2002 6330 6337
32. C. Scherfer, H. Tang, Z. Kambris, N. Lhocine, C. Hashimoto, and B. Lemaitre Drosophila serpin-28D regulates hemolymph phenoloxidase activity and adult pigmentation Dev. Biol. 2008
33. H. Tang, Z. Kambris, B. Lemaitre, and C. Hashimoto A serpin that regulates immune melanization in the respiratory system of Drosophila Dev. Cell 15 2008 617 626
34. S.T. Ahmad, S.T. Sweeney, J.A. Lee, N.T. Sweeney, and F.B. Gao 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 106 2009 12168 12173
35. P. Ligoxygakis, S. Roth, and J.M. Reichhart A serpin regulates dorsal-ventral axis formation in the Drosophila embryo Curr. Biol. 13 2003 2097 2102
36. C. Hashimoto, D.R. Kim, L.A. Weiss, J.W. Miller, and D. Morisato Spatial regulation of developmental signaling by a serpin Dev. Cell 5 2003 945 950
37. M.J. Richer, C.A. Keays, J. Waterhouse, J. Minhas, C. Hashimoto, and F. Jean The Spn4 gene of Drosophila encodes a potent furin-directed secretory pathway serpin Proc. Natl. Acad. Sci. U S A 101 2004 10560 10565
38. M. Bruning, M. Lummer, C. Bentele, M.M. Smolenaars, K.W. Rodenburg, and H. Ragg The Spn4 gene from Drosophila melanogaster is a multipurpose defence tool directed against proteases from three different peptidase families Biochem. J. 401 2007 325 331
39. S.L. Stroschein-Stevenson, E. Foley, P.H. O'Farrell, and A.D. Johnson Identification of Drosophila gene products required for phagocytosis of Candida albicans PLoS Biol. 4 2006 e4
40. M. Lagueux, E. Perrodou, E.A. Levashina, M. Capovilla, and J.A. Hoffmann Constitutive expression of a complement-like protein in toll and JAK gain-of-function mutants of Drosophila Proc. Natl. Acad. Sci. U S A 97 2000 11427 11432
41. E. De Gregorio, P.T. Spellman, G.M. Rubin, and B. Lemaitre Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays Proc. Natl. Acad. Sci. U S A 98 2001 12590 12595
42. N. Buchon, N.A. Broderick, M. Poidevin, S. Pradervand, and B. Lemaitre Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation Cell Host Microbe 5 2009 200 211
43. T.L. Jacobsen, D. Cain, L. Paul, S. Justiniano, A. Alli, J.S. Mullins, C.P. Wang, J.P. Butchar, and A. Simcox Functional analysis of genes differentially expressed in the Drosophila wing disc: role of transcripts enriched in the wing region Genetics 174 2006 1973 1982
44. R.B. Beckstead, G. Lam, and C.S. Thummel Specific transcriptional responses to juvenile hormone and ecdysone in Drosophila Insect Biochem. Mol. Biol. 37 2007 570 578
45. Y. Li, and J. Tower Adult-specific over-expression of the Drosophila genes magu and hebe increases life span and modulates late-age female fecundity Mol. Genet. Genomics 281 2009 147 162
46. J. Pentek, L. Parker, A. Wu, and K. Arora Follistatin preferentially antagonizes activin rather than BMP signaling in Drosophila Genesis 47 2009 261 273
47. T. Niimi, H. Yokoyama, A. Goto, K. Beck, and Y. Kitagawa A Drosophila gene encoding multiple splice variants of Kazal-type serine protease inhibitor-like proteins with potential destinations of mitochondria, cytosol and the secretory pathway Eur. J. Biochem. 266 1999 282 292
48. N. Ramesh, M. Sugumaran, and J.E. Mole Purification and characterization of two trypsin inhibitors from the hemolymph of Manduca sexta larvae J. Biol. Chem. 263 1988 11523 11527
49. X. Nirmala, D. Kodrik, M. Zurovec, and F. Sehnal Insect silk contains both a Kunitz-type and a unique Kazal-type proteinase inhibitor Eur. J. Biochem. 268 2001 2064 2073
50. A. Kurioka, M. Yamazaki, and H. Hirano Primary structure and possible functions of a trypsin inhibitor of Bombyx mori Eur. J. Biochem. 259 1999 120 126
51. I.M. Francischetti, J.G. Valenzuela, J.F. Andersen, T.N. Mather, and J.M. Ribeiro Ixolaris, a novel recombinant tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick, Ixodes scapularis: identification of factor X and factor Xa as scaffolds for the inhibition of factor VIIa/tissue factor complex Blood 99 2002 3602 3612
52. T. Hamamoto, M. Yamamoto, O. Nordfang, J.G. Petersen, D.C. Foster, and W. Kisiel Inhibitory properties of full-length and truncated recombinant tissue factor pathway inhibitor (TFPI). Evidence that the third Kunitz-type domain of TFPI is not essential for the inhibition of factor VIIa-tissue factor complexes on cell surfaces J. Biol. Chem. 268 1993 8704 8710
53. S.M. Ceraul, S.M. Dreher-Lesnick, A. Mulenga, M.S. Rahman, and A.F. Azad Functional characterization and novel rickettsiostatic effects of a Kunitz-type serine protease inhibitor from the tick Dermacentor variabilis Infect. Immun. 76 2008 5429 5435
54. Z. Zou, Z. Picheng, H. Weng, K. Mita, and H. Jiang A comparative analysis of serpin genes in the silkworm genome Genomics 93 2009 367 375
55. R. Jiang, E.H. Kim, J.H. Gong, H.M. Kwon, C.H. Kim, K.H. Ryu, J.W. Park, K. Kurokawa, J. Zhang, D. Gubb, and B.L. Lee Three pairs of protease-serpin complexes cooperatively regulate the insect innate immune responses J. Biol. Chem. 284 2009 35652 35658
56. T. Sasaki Patchwork-structure serpins from silkworm (Bombyx mori) larval hemolymph Eur. J. Biochem. 202 1991 255 261
57. H. Jiang, and M.R. Kanost Characterization and functional analysis of 12 naturally occurring reactive site variants of serpin-1 from Manduca sexta J. Biol. Chem. 272 1997 1082 1087
58. A. Danielli, F.C. Kafatos, and T.G. Loukeris Cloning and characterization of four Anopheles gambiae serpin isoforms, differentially induced in the midgut by Plasmodium berghei invasion J. Biol. Chem. 278 2003 4184 4193
59. O. Kruger, J. Ladewig, K. Koster, and H. Ragg Widespread occurrence of serpin genes with multiple reactive centre-containing exon cassettes in insects and nematodes Gene 293 2002 97 105
60. S. Borner, and H. Ragg Functional diversification of a protease inhibitor gene in the genus Drosophila and its molecular basis Gene 415 2008 23 31
61. D.J. Askew, Y.S. Askew, Y. Kato, R.F. Turner, K. Dewar, J. Lehoczky, and G.A. Silverman Comparative genomic analysis of the clade B serpin cluster at human chromosome 18q21: amplification within the mouse squamous cell carcinoma antigen gene locus Genomics 84 2004 176 184
62. D.J. Askew, P. Coughlin, and P.I. Bird Mouse serpins and transgenic studies G.A. Silverman, D.A. Lomas, Molecular and Cellular Aspects of the Serpinopathies and Disorders in Serpin Activity 2007 Singapore
63. D. Kaiserman, and P.I. Bird Analysis of vertebrate genomes suggests a new model for clade B serpin evolution BMC Genomics 6 2005 167
64. J.D. Inglis, and R.E. Hill The murine Spi-2 proteinase inhibitor locus: a multigene family with a hypervariable reactive site domain EMBO J. 10 1991 255 261
65. R.H. Law, Q. Zhang, S. McGowan, A.M. Buckle, G.A. Silverman, W. Wong, C.J. Rosado, C.G. Langendorf, R.N. Pike, P.I. Bird, and J.C. Whisstock An overview of the serpin superfamily Genome Biol. 7 2006 216
66. J.A. Hoffmann, and J.M. Reichhart Drosophila innate immunity: an evolutionary perspective Nat. Immunol. 3 2002 121 126
67. M. Gottar, V. Gobert, A.A. Matskevich, J.M. Reichhart, C. Wang, T.M. Butt, M. Belvin, J.A. Hoffmann, and D. Ferrandon Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors Cell 127 2006 1425 1437
68. M. Yamasaki, W. Li, D.J. Johnson, and J.A. Huntington Crystal structure of a stable dimer reveals the molecular basis of serpin polymerization Nature 455 2008 1255 1258
69. C. Green, G. Brown, T.R. Dafforn, J.M. Reichhart, T. Morley, D.A. Lomas, and D. Gubb Drosophila necrotic mutations mirror disease-associated variants of human serpins Development 130 2003 1473 1478
70. R. Carrell, and J. Corral What can Drosophila tell us about serpins, thrombosis and dementia? Bioessays 26 2004 1 5
71. C. Green, E. Levashina, C. McKimmie, T. Dafforn, J.M. Reichhart, and D. Gubb The necrotic gene in Drosophila corresponds to one of a cluster of three serpin transcripts mapping at 43A1.2 Genetics 156 2000 1117 1127
72. X.Q. Yu, H. Jiang, Y. Wang, and M.R. Kanost Nonproteolytic serine proteinase homologs are involved in prophenoloxidase activation in the tobacco hornworm, Manduca sexta Insect Biochem. Mol. Biol. 33 2003 197 208
73. M.Z. Kounnas, F.C. Church, W.S. Argraves, and D.K. Strickland Cellular internalization and degradation of antithrombin III-thrombin, heparin cofactor II-thrombin, and alpha 1-antitrypsin-trypsin complexes is mediated by the low density lipoprotein receptor-related protein J. Biol. Chem. 271 1996 6523 6529
74. A. Kasza, H.H. Petersen, C.W. Heegaard, K. Oka, A. Christensen, A. Dubin, L. Chan, and P.A. Andreasen Specificity of serine proteinase/serpin complex binding to very-low-density lipoprotein receptor and alpha2-macroglobulin receptor/low-density-lipoprotein-receptor-related protein Eur. J. Biochem. 248 1997 270 281
75. S.F. Soukup, J. Culi, and D. Gubb Uptake of the necrotic serpin in Drosophila melanogaster via the lipophorin receptor-1 PLoS Genet. 5 2009 e1000532
76. C. Owa, F. Aoki, and M. Nagata Protein degradation in silkworm peritracheal athrocytes and its physiological role in metamorphosis J. Insect Physiol. 2010
77. H. Weavers, S. Prieto-Sanchez, F. Grawe, A. Garcia-Lopez, R. Artero, M. Wilsch-Brauninger, M. Ruiz-Gomez, H. Skaer, and B. Denholm The insect nephrocyte is a podocyte-like cell with a filtration slit diaphragm Nature 457 2009 322 326
78. N. Jiang, S. Thangamani, C.F. Chor, S.Y. Wang, I. Winarsih, R.J. Du, J. Sivaraman, B. Ho, and J.L. Ding A novel serine protease inhibitor acts as an immunomodulatory switch while maintaining homeostasis J. Innate Immun. 1 2009 465 479
79. H. Jiang, A.B. Mulnix, and M.R. Kanost Expression and characterization of recombinant Manduca sexta serpin-1B and site-directed mutants that change its inhibitory selectivity Insect Biochem. Mol. Biol. 25 1995 1093 1100
80. N.D. Rawlings, and F.R. Morton The MEROPS batch BLAST: a tool to detect peptidases and their non-peptidase homologues in a genome Biochimie 90 2008 243 259
81. H. Jiang, Y. Wang, X.Q. Yu, and M.R. Kanost Prophenoloxidase-activating proteinase-2 from hemolymph of Manduca sexta. A bacteria-inducible serine proteinase containing two clip domains J. Biol. Chem. 278 2003 3552 3561
82. H. Kan, C.H. Kim, H.M. Kwon, J.W. Park, K.B. Roh, H. Lee, B.J. Park, R. Zhang, J. Zhang, K. Soderhall, N.C. Ha, and B.L. Lee Molecular control of phenoloxidase-induced melanin synthesis in an insect J. Biol. Chem. 283 2008 25316 25323
83. B. Murugasu-Oei, V. Rodrigues, X. Yang, and W. Chia Masquerade: a novel secreted serine protease-like molecule is required for somatic muscle attachment in the Drosophila embryo Genes Dev. 9 1995 139 154